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TONG-CHUAN HE

TitleASSOCIATE PROFESSOR
InstitutionUniversity of Chicago
DepartmentOrthopaedic Surg & Rehab Med
AddressChicago IL 60637
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    Collapse Overview 
    Collapse overview
    I direct the Molecular Oncology Laboratory in the Department of Orthopaedic Surgery and Rehabilitation Medicine. Our lab consists of a dynamic group of basic science investigators and physician scientists, who have diverse expertise and a broad range of research interests. Our shared long-term objective is to better understand the molecular pathogenesis of bone and musculoskeletal diseases and to translate basic discoveries into potential therapies and/or preventive measures in clinical settings. Specifically, we focus on the following areas:

    LINEAGE COMMITMENT AND TERMINAL DIFFERENTIATION OF MESENCHYMAL STEM CELLS (MSCS)

    Multipotency of MSCs
    MSCs are pluripotent and capable of differentiating into osteogenic, chondrogenic, myogenic or adipogenic lineage. Understanding the molecular mechanisms of bone formation is pivotal for studying the pathogenesis of bone diseases. We are interested in elucidating the molecular mechanisms through which regulate the proliferation and differentiation of osteoblasts, chondrocytes, and adipocytes. Both Wnt/beta-catenin and bone morphogenetic proteins (BMPs) have been considered as important regulators of osteogenic differentiation of mesenchymal stem cells. We are investigating the biological functions of BMPs and Wnt/beta-catenin signaling in regulating the osteoblast differentiation of MSCs. We have therefore conducted a comprehensive analysis of BMP and Wnt3A-induced osteoblast differentiation of MSCs. Our findings indicate that osteoblast differentiation is a well-regulated process in normal progenitor cells, while osteosarcoma cells are refractory to osteogenic differentiation signal.

    BMP-9 is one of the most potent regulators of osteogenic differentiation
    The bone-forming osteoblasts are derived from pluripotent bone marrow fibroblasts (a.k.a., MSCs). Although the molecular mechanisms underlying bone formation remain to be defined, BMPs seem to play an important role in osteoblast differentiation. At least 15 types of BMPs have been identified in mice and humans. However, the ability of BMPs to induce osteoblast differentiation of mesenchymal stem cells has not been comprehensively investigated, mostly due to the fact that recombinant proteins are either not biologically active or not available for all BMPs. Through a comprehensive analysis, we found that BMP2, BMP6, and BMP9 (to a much lesser extent, BMP4 and BMP7) exhibited the greatest ability to induce osteoblast differentiation, whereas BMP3 was shown to inhibit osteogenesis, both in vitro and in vivo. Our findings about BMP9 as one of the most potent inducers of osteoblast differentiation are novel and particularly intriguing because BMP9 is one of the least characterized BMPs and its functions are largely unknown. Thus, many questions regarding BMP9 signaling need to be answered: What are the type I and type II TGFbeta/BMP receptors involved in BMP9 binding? What Smads are required for BMP9 signaling? How are the downstream targets regulated by BMP9? More importantly, what are the roles of BMP9 during embryonic and/or skeletal development? We are interested in addressing these questions.

    Critical mediators of BMP-induced differentiation of MSCs
    We have identified several potentially important signaling mediators of BMP-induced osteogenic differentiation. These targets include the Inhibitors of DNA binding/Differentiation helix-loop-helix (a.k.a., Id proteins) and CTGF. Interestingly, both Ids and CTGF have been shown to overexpress in human tumors. Our findings suggest that Ids and CTGF may play an important role in promoting the proliferation of early osteoblast progenitor cells and that their expression must be down-regulated during the terminal differentiation of committed osteoblasts, suggesting that a balanced regulation of their expression may be critical to BMP-induced osteoblast lineage-specific differentiation of MSCs. We are currently dissecting the functional roles of the important downstream mediators in BMP-induced osteogenic signaling. We are also interested in identifying the molecular switches that control the lineage-specific differentiation of osteoblasts, chondrocytes, and adipocytes in MSCs. We are especially interested in understanding at what stage osteogenic BMPs (e.g., BMP2 or BMP9)-induced osteogenic and adipogenic differentiation diverges. What are the potential regulators that control this lineage divergence? It has been long postulated that a disrupted balance between osteogenesis and adipogenesis may cause musculoskeletal diseases, such as osteoporosis.

    Wnts regulate osteogenic differentiation of mesenchymal stem cells
    Our earlier studies demonstrated that Wnt/beta-catenin signaling is de-regulated in over 70% of human osteosarcoma. Recent studies also suggest that Wnt signaling may play an important role in regulating bone density, and one of the Wnt signaling antagonists Dkk1 may be implicated in the development of osteolytic lesion in multiple myeloma patients. We demonstrated that Wnt3A can induce the early osteogenic marker alkaline phosphatase in MSCs. Upon analyzing the gene expression profile of MSCs that were stimulated with Wnt3A, we found that three members of the CCN family, CCN1/Cyr61, CCN2/CTGF, and CCN5/WISP2, were among the most significantly up-regulated genes. Further studies demonstrate that CTGF is a mutual target of Wnt and BMP-9, and plays an important role in regulating osteogenic differentiation. However, more questions remain to be answered. We are currently investigating how osteogenic differentiation of MSCs is regulated by canonical and non-canonical Wnt signaling.

    MOLECULAR BASES OF BONE AND SOFT TISSUE SARCOMAS

    Sarcomas represent a heterogeneous group of malignant mesenchymal tumors with numerous histologic subtypes and complex cytogenetic abnormalities. Unlike other common solid tumors, sarcomas are relatively uncommon and their molecular pathogenesis, in general, are poorly understood. We mainly focus on understanding the molecular biology of primary bone tumor (a.k.a., osteosarcoma, OS). Osteosarcoma is the most common primary malignancy of bone, and is among the most common non-hematological primary tumors of bone in both children and adults. The peak incidence occurs in the second decade. With preoperative chemotherapy, the five-year survival rate of patients with non-metastatic tumors has improved significantly to approximately 60-70%. However, cases with local recurrence and/or pulmonary metastasis are usually less sensitive, if not resistant, to conventional chemotherapies. Several cytogenetic studies suggest that certain chromosomal regions may be amplified, rearranged, or deleted in some, but not all, human osteosarcomas. Unfortunately, the low incidence of this disease and the absence of any familial predisposition have complicated efforts to identify osteosarcoma-associated genes. Thus, we are taking a comprehensive approach to elucidate the molecular mechanisms underlying the development of osteosarcoma.

    Wnt/beta-catenin signaling in the development of human osteosarcoma
    Aberrant activation of Wnt/beta-catenin signaling by inactivating APC tumor suppressor or oncogenic activation of beta-catenin plays an important role in colorectal tumorigenesis. Oncogenic activation of beta-catenin has also been reported in several types of human solid tumors. We found that beta-catenin signaling is de-regulated in about 70% of human osteosarcoma without beta-catenin mutations. As in many other types of non-colon cancer, little is known about how Wnt/beta-catenin signaling pathway is activated. Therefore, we are interested in elucidating the upstream regulatory mechanisms that may underline of the beta-catenin signaling pathway. We are also interested in investigating the possible pathogenic role of beta-catenin deregulation in bone and soft tissue tumors. Furthermore, we are investigating the potential roles of EF-hand calcium-binding S100 proteins in osteosarcoma progression and the development of pulmonary metastasis.

    Clinically relevant osteosarcoma animal model
    In order to investigate the pathogenesis of human osteosarcoma, there is a great need to develop a clinically relevant animal model. We have developed such an orthotopic animal model of osteosarcoma using several human osteosarcoma lines. This clinically relevant model of human osteosarcoma provides varying degrees of tumor growth at the primary site and of metastatic potential. Thus, this orthotopic model is being used as a valuable tool to investigate factors that promote or inhibit osteosarcoma growth and/or metastasis. For instance, we are now using this model to investigate the roles of genes that are known to promote cell proliferation and inhibit differentiation, and genes that potentially promote or inhibit cancer metastasis. This orthotopic model can also be used to test anti-tumor small molecules or other targeted therapies.

    Osteosarcoma is a differentiation disease
    We believe that understanding the molecular events behind normal osteoblast differentiation of MSCs may provide important clues to osteosarcoma development. Stem cell differentiation and tumorigenesis share some strikingly similar characteristics. Both normal stem cells and cancer stem cells have the ability to self-renew. Although stem cells are often the target of genetic events that are necessary or sufficient for malignant transformation, in some cases restricted progenitors or even differentiated cells may become transformed. Thus, cancer stem cells may be derived from tissue-specific stem cells or progenitors, such as MSCs. Although cancer stem cells for osteosarcoma remain to be identified, OS cells indeed exhibit the characteristics of undifferentiated osteoblasts, and we have shown that differentiation-promoting agents can inhibit OS proliferation. Accordingly, we found that human osteosarcoma cells are in general refractory to osteogenic BMPs and exhibit no signs of terminal differentiation upon osteogenic BMP stimulation. Thus, we hypothesize that osteosarcoma development is caused by molecular/genetic disruptions of the osteogenic differentiation pathway. We are investigating and identifying the possible defects in osteogenic pathway, including the possible roles of the early target genes of BMP-induced osteoblast lineage-specific differentiation of MSCs.

    MOLECULAR BIOLOGY OF CANCER METASTASIS

    Cancer metastasis is an often overlooked and least understood problem. Metastasis is defined as the progressive growth of tumor cells at a site that is discontinuous from the primary tumor. Although not an efficient process, colonization at distant tissues by tumor cells represents the most dangerous attribute of cancer, because metastases, rather than primary tumors, are responsible for most cancer deaths. Metastatic cells are a subset of primary tumor cells that have acquired the ability to complete a multi-step metastatic cascade, including migration, dissemination, extravasation, and eventual proliferation at a discontinuous secondary site. Understanding the molecular biology of cancer metastasis may provide novel intervention strategies to control/contain metastatic lesions, and/or to improve the quality of life for the patients with these advanced diseases.

    Pulmonary metastasis of primary bone tumors
    Lung metastasis is the leading cause of OS mortality. Our orthotopic tumor model of human OS provides a unique opportunity for us to investigate the molecular events underlying osteosarcoma pulmonary metastasis. Using this model, we have conducted serial selections of highly metastatic human OS sublines, which were otherwise non-metastatic. Using microarray analysis, we have compared the gene expression profiles between these sublines and the parental lines in search for gene(s) that may cause or be associated with osteosarcoma metastasis. In an alternative approach, we are conducting functional selection assays, in which an RNAi library has been introduced into the non-metastatic or less metastatic human osteosarcoma cells to recover lung metastases and to identify potential metastasis suppressors of human osteosarcoma.

    Metastatic bone tumors
    Bone is one of the most frequently targeted organs for cancer metastasis, and bone is the most common site for distant relapse of most cancers. The bone microenvironment is unique among metastatic target tissues because it is subjected to continuous remodeling under the influence circulating hormones and local bone-derived factors. Interactions between the bone microenvironment and the cancer cells can give rise to osteolytic (bone resorbing) or osteoblastic (bone forming) metastasis. Osteolytic bone metastasis are characteristic for most malignancies, such as breast cancer and lung cancer, while osteoblastic metastasis is mostly associated with prostate cancer. We are investigating the molecular mechanisms through which the interactions between metastatic (breast and prostate) cancer cells and bone microenvironment are regulated.

    NOVEL THERAPEUTIC AND/OR PREVENTIVE STRATEGIES FOR BONE AND MUSCULOSKELETAL DISEASES

    The ultimate goal of biomedical research is to develop innovative diagnostic, therapeutic, and/or preventive strategies for human diseases. We are interested in developing innovative approaches for local or systemic delivery of therapeutic genes as effective treatment for bone and musculoskeletal diseases. We are investigating the use of osteogenic BMPs for bone regeneration, enhancing fracture healing, repairing segmental defects, promoting spinal fusion, and preventing implant wear particle-induced osteolysis. We have recently demonstrated the potential use of some of the BMPs in promoting biomechanical features of healing tendons/ligaments. We also demonstrated that Sox9, a master regulator of chondrogenesis, may be used in gene therapy to treat intervertebral disc degeneration and articular cartilage injuries. These lines of investigation reflect our commitment to the true spirit of translational research in bone and musculoskeletal disorders.


    Collapse Biography 
    Collapse education and training
    Chongqing Medical University, Chongqing, ChinaB.M (MD equivalent)07/1984Medicine
    Chongqing Medical University, Chongqing, ChinaMSc07/1987Biochemistry
    The Pennsylvania State University, University Park, PAPhD12/1994Molecular Cell Biology
    HHMI/Johns Hopkins School of Medicine, Baltimore, MDPostdoc11/1999Cancer Biology/Genetics

    Collapse Presentations, Websites, Twitter, Videos 
    Collapse Websites

    Collapse Bibliographic 
    Collapse selected publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
    List All   |   Timeline
    1. Wang CZ, Huang WH, Zhang CF, Wan JY, Wang Y, Yu C, Williams S, He TC, Du W, Musch MW, Chang EB, Yuan CS. Role of intestinal microbiome in American ginseng-mediated colon cancer protection in high fat diet-fed AOM/DSS mice. Clin Transl Oncol. 2017 Aug 14. PMID: 28808878.
      View in: PubMed
    2. Pakvasa M, Alverdy A, Mostafa S, Wang E, Fu L, Li A, Oliveira L, Athiviraham A, Lee MJ, Wolf JM, He TC, Ameer GA, Reid RR. Neural EGF-like protein 1 (NELL-1): Signaling crosstalk in mesenchymal stem cells and applications in regenerative medicine. Genes Dis. 2017 Sep; 4(3):127-137. PMID: 29276737.
      View in: PubMed
    3. Zhang ZC, Liu JX, Shao ZW, Pu FF, Wang BC, Wu Q, Zhang YK, Zeng XL, Guo XD, Yang SH, He TC. In vitro effect of microRNA-107 targeting Dkk-1 by regulation of Wnt/ß-catenin signaling pathway in osteosarcoma. Medicine (Baltimore). 2017 Jul; 96(27):e7245. PMID: 28682874.
      View in: PubMed
    4. Shui YM, Lv GY, Shan LT, Fan CL, Tian N, Zhang L, He TC, Gao JL. Epimedin C Promotes Vascularization During BMP2-Induced Osteogenesis and Tumor-Associated Angiogenesis. Am J Chin Med. 2017 Jun 28; 1-19. PMID: 28659032.
      View in: PubMed
    5. Liao J, Yu X, Hu X, Fan J, Wang J, Zhang Z, Zhao C, Zeng Z, Shu Y, Zhang R, Yan S, Li Y, Zhang W, Cui J, Ma C, Li L, Yu Y, Wu T, Wu X, Lei J, Wang J, Yang C, Wu K, Wu Y, Tang J, He BC, Deng ZL, Luu HH, Haydon RC, Reid RR, Lee MJ, Wolf JM, Huang W, He TC. lncRNA H19 mediates BMP9-induced osteogenic differentiation of mesenchymal stem cells (MSCs) through Notch signaling. Oncotarget. 2017 Jun 27. PMID: 28668938.
      View in: PubMed
    6. Liao J, Yu X, Hu X, Fan J, Wang J, Zhang Z, Zhao C, Zeng Z, Shu Y, Zhang R, Yan S, Li Y, Zhang W, Cui J, Ma C, Li L, Yu Y, Wu T, Wu X, Lei J, Wang J, Yang C, Wu K, Wu Y, Tang J, He BC, Deng ZL, Luu HH, Haydon RC, Reid RR, Lee MJ, Wolf JM, Huang W, He TC. lncRNA H19 mediates BMP9-induced osteogenic differentiation of mesenchymal stem cells (MSCs) through Notch signaling. Oncotarget. 2017 Aug 08; 8(32):53581-53601. PMID: 28881833.
      View in: PubMed
    7. Wang T, Zhang Z, Wang K, Wang J, Jiang Y, Xia J, Gou L, Liu M, Zhou L, He T, Zhang Y. Inhibitory effects of BMP9 on breast cancer cells by regulating their interaction with pre-adipocytes/adipocytes. Oncotarget. 2017 May 30; 8(22):35890-35901. PMID: 28415788.
      View in: PubMed
    8. Zou Y, Qazvini NT, Zane K, Sadati M, Wei Q, Liao J, Fan J, Song D, Liu J, Ma C, Qu X, Chen L, Yu X, Zhang Z, Zhao C, Zeng Z, Zhang R, Yan S, Wu T, Wu X, Shu Y, Li Y, Zhang W, Reid RR, Lee MJ, Wolf JM, Tirrell M, He TC, de Pablo JJ, Deng ZL. Gelatin-Derived Graphene-Silicate Hybrid Materials Are Biocompatible and Synergistically Promote BMP9-Induced Osteogenic Differentiation of Mesenchymal Stem Cells. ACS Appl Mater Interfaces. 2017 May 17; 9(19):15922-15932. PMID: 28406027.
      View in: PubMed
    9. Song D, Zhang F, Reid RR, Ye J, Wei Q, Liao J, Zou Y, Fan J, Ma C, Hu X, Qu X, Chen L, Li L, Yu Y, Yu X, Zhang Z, Zhao C, Zeng Z, Zhang R, Yan S, Wu T, Wu X, Shu Y, Lei J, Li Y, Zhang W, Wang J, Lee MJ, Wolf JM, Huang D, He TC. BMP9 induces osteogenesis and adipogenesis in the immortalized human cranial suture progenitors from the patent sutures of craniosynostosis patients. J Cell Mol Med. 2017 Nov; 21(11):2782-2795. PMID: 28470873.
      View in: PubMed
    10. Liao J, Wei Q, Fan J, Zou Y, Song D, Liu J, Liu F, Ma C, Hu X, Li L, Yu Y, Qu X, Chen L, Yu X, Zhang Z, Zhao C, Zeng Z, Zhang R, Yan S, Wu T, Wu X, Shu Y, Lei J, Li Y, Zhang W, Wang J, Reid RR, Lee MJ, Huang W, Wolf JM, He TC, Wang J. Characterization of retroviral infectivity and superinfection resistance during retrovirus-mediated transduction of mammalian cells. Gene Ther. 2017 Jun; 24(6):333-341. PMID: 28387759.
      View in: PubMed
    11. Wei Q, Fan J, Liao J, Zou Y, Song D, Liu J, Cui J, Liu F, Ma C, Hu X, Li L, Yu Y, Qu X, Chen L, Yu X, Zhang Z, Zhao C, Zeng Z, Zhang R, Yan S, Wu X, Shu Y, Reid RR, Lee MJ, Wolf JM, He TC. Engineering the Rapid Adenovirus Production and Amplification (RAPA) Cell Line to Expedite the Generation of Recombinant Adenoviruses. Cell Physiol Biochem. 2017; 41(6):2383-2398. PMID: 28463838.
      View in: PubMed
    12. Lee CS, Bishop ES, Zhang R, Yu X, Farina EM, Yan S, Zhao C, Zheng Z, Shu Y, Wu X, Lei J, Li Y, Zhang W, Yang C, Wu K, Wu Y, Ho S, Athiviraham A, Lee MJ, Wolf JM, Reid RR, He TC. Adenovirus-Mediated Gene Delivery: Potential Applications for Gene and Cell-Based Therapies in the New Era of Personalized Medicine. Genes Dis. 2017 Jun; 4(2):43-63. PMID: 28944281.
      View in: PubMed
    13. Xue Q, Yang JF, Li B, He TC, Zhang BQ. [Regulatory effect of faciogenital dysplasia 6 gene on hepatic stem cell differentiation]. Zhonghua Gan Zang Bing Za Zhi. 2017 Apr 20; 25(4):268-272. PMID: 28494545.
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    14. Fan J, Wei Q, Liao J, Zou Y, Song D, Xiong D, Ma C, Hu X, Qu X, Chen L, Li L, Yu Y, Yu X, Zhang Z, Zhao C, Zeng Z, Zhang R, Yan S, Wu T, Wu X, Shu Y, Lei J, Li Y, Zhang W, Haydon RC, Luu HH, Huang A, He TC, Tang H. Noncanonical Wnt signaling plays an important role in modulating canonical Wnt-regulated stemness, proliferation and terminal differentiation of hepatic progenitors. Oncotarget. 2017 Apr 18; 8(16):27105-27119. PMID: 28404920.
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    15. Liu JX, Zhang ZC, Shao ZW, Pu FF, Wang BC, Zhang YK, Zeng XL, Guo XD, Yang SH, He TC. TRAIL-R1 as a novel surface marker for circulating giant cell tumor of bone. Oncotarget. 2017 Aug 01; 8(31):50724-50730. PMID: 28881598.
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    16. Liao J, Wei Q, Zou Y, Fan J, Song D, Cui J, Zhang W, Zhu Y, Ma C, Hu X, Qu X, Chen L, Yu X, Zhang Z, Wang C, Zhao C, Zeng Z, Zhang R, Yan S, Wu T, Wu X, Shu Y, Lei J, Li Y, Luu HH, Lee MJ, Reid RR, Ameer GA, Wolf JM, He TC, Huang W. Notch Signaling Augments BMP9-Induced Bone Formation by Promoting the Osteogenesis-Angiogenesis Coupling Process in Mesenchymal Stem Cells (MSCs). Cell Physiol Biochem. 2017; 41(5):1905-1923. PMID: 28384643.
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    17. Dumanian ZP, Tollemar V, Ye J, Lu M, Zhu Y, Liao J, Ameer GA, He TC, Reid RR. Repair of critical sized cranial defects with BMP9-transduced calvarial cells delivered in a thermoresponsive scaffold. PLoS One. 2017; 12(3):e0172327. PMID: 28249039.
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    18. Zhu P, Wu F, Mosenson J, Zhang H, He TC, Wu WS. CRISPR/Cas9-Mediated Genome Editing Corrects Dystrophin Mutation in Skeletal Muscle Stem Cells in a Mouse Model of Muscle Dystrophy. Mol Ther Nucleic Acids. 2017 Jun 16; 7:31-41. PMID: 28624206.
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    19. Zhang F, Li Y, Zhang H, Huang E, Gao L, Luo W, Wei Q, Fan J, Song D, Liao J, Zou Y, Liu F, Liu J, Huang J, Guo D, Ma C, Hu X, Li L, Qu X, Chen L, Yu X, Zhang Z, Wu T, Luu HH, Haydon RC, Song J, He TC, Ji P. Anthelmintic mebendazole enhances cisplatin's effect on suppressing cell proliferation and promotes differentiation of head and neck squamous cell carcinoma (HNSCC). Oncotarget. 2017 Feb 21; 8(8):12968-12982. PMID: 28099902.
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    20. Wang J, Liao J, Zhang F, Song D, Lu M, Liu J, Wei Q, Tang S, Liu H, Fan J, Zou Y, Guo D, Huang J, Liu F, Ma C, Hu X, Li L, Qu X, Chen L, Weng Y, Lee MJ, He TC, Reid RR, Zhang J. NEL-Like Molecule-1 (Nell1) Is Regulated by Bone Morphogenetic Protein 9 (BMP9) and Potentiates BMP9-Induced Osteogenic Differentiation at the Expense of Adipogenesis in Mesenchymal Stem Cells. Cell Physiol Biochem. 2017; 41(2):484-500. PMID: 28214873.
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    21. Lu M, Liao J, Dong J, Wu J, Qiu H, Zhou X, Li J, Jiang D, He TC, Quan Z. An effective treatment of experimental osteomyelitis using the antimicrobial titanium/silver-containing nHP66 (nano-hydroxyapatite/polyamide-66) nanoscaffold biomaterials. Sci Rep. 2016 Dec 16; 6:39174. PMID: 27982110.
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    22. Gao JL, Shui YM, Jiang W, Huang EY, Shou QY, Ji X, He BC, Lv GY, He TC. Hypoxia pathway and hypoxia-mediated extensive extramedullary hematopoiesis are involved in ursolic acid's anti-metastatic effect in 4T1 tumor bearing mice. Oncotarget. 2016 Nov 01; 7(44):71802-71816. PMID: 27708244.
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    23. Zhang F, Song J, Zhang H, Huang E, Song D, Tollemar V, Wang J, Wang J, Mohammed M, Wei Q, Fan J, Liao J, Zou Y, Liu F, Hu X, Qu X, Chen L, Yu X, Luu HH, Lee MJ, He TC, Ji P. Wnt and BMP Signaling Crosstalk in Regulating Dental Stem Cells: Implications in Dental Tissue Engineering. Genes Dis. 2016 Dec; 3(4):263-276. PMID: 28491933.
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    24. Lyon SM, Mayampurath A, Rogers MR, Wolfgeher DJ, Fisher SM, Volchenboum SL, He TC, Reid RR. A method for whole protein isolation from human cranial bone. Anal Biochem. 2016 Dec 15; 515:33-39. PMID: 27677936.
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    25. Lu S, Wang J, Ye J, Zou Y, Zhu Y, Wei Q, Wang X, Tang S, Liu H, Fan J, Zhang F, Farina EM, Mohammed MM, Song D, Liao J, Huang J, Guo D, Lu M, Liu F, Liu J, Li L, Ma C, Hu X, Lee MJ, Reid RR, Ameer GA, Zhou D, He T. Bone morphogenetic protein 9 (BMP9) induces effective bone formation from reversibly immortalized multipotent adipose-derived (iMAD) mesenchymal stem cells. Am J Transl Res. 2016; 8(9):3710-3730. PMID: 27725853.
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    26. Uchiyama K, Sakiyama T, Hasebe T, Musch MW, Miyoshi H, Nakagawa Y, He TC, Lichtenstein L, Naito Y, Itoh Y, Yoshikawa T, Jabri B, Stappenbeck T, Chang EB. Butyrate and bioactive proteolytic form of Wnt-5a regulate colonic epithelial proliferation and spatial development. Sci Rep. 2016 Aug 26; 6:32094. PMID: 27561676.
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    27. Zhao B, Shah P, Qiang L, He TC, Budanov A, He YY. Distinct Role of Sesn2 in Response to UVB-Induced DNA Damage and UVA-Induced Oxidative Stress in Melanocytes. Photochem Photobiol. 2017 Jan; 93(1):375-381. PMID: 27463837.
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    28. Deng Y, Wang Z, Zhang F, Qiao M, Yan Z, Wei Q, Wang J, Liu H, Fan J, Zou Y, Liao J, Hu X, Chen L, Yu X, Haydon RC, Luu HH, Qi H, He TC, Zhang J. A Blockade of IGF Signaling Sensitizes Human Ovarian Cancer Cells to the Anthelmintic Niclosamide-Induced Anti-Proliferative and Anticancer Activities. Cell Physiol Biochem. 2016; 39(3):871-88. PMID: 27497986.
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    29. Li H, Yuan SM, Yang M, Zha H, Li XR, Sun H, Duan L, Gu Y, Li AF, Weng YG, Luo JY, He TC, Wang Y, Li CY, Li FQ, Wang ZB, Zhou L. High intensity focused ultrasound inhibits melanoma cell migration and metastasis through attenuating microRNA-21-mediated PTEN suppression. Oncotarget. 2016 Aug 02; 7(31):50450-50460. PMID: 27391071.
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    30. Ren X, Weisgerber DW, Bischoff D, Lewis MS, Reid RR, He TC, Yamaguchi DT, Miller TA, Harley BA, Lee JC. Nanoparticulate Mineralized Collagen Scaffolds and BMP-9 Induce a Long-Term Bone Cartilage Construct in Human Mesenchymal Stem Cells. Adv Healthc Mater. 2016 Jul; 5(14):1821-30. PMID: 27275929.
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    31. Ye J, Wang J, Zhu Y, Wei Q, Wang X, Yang J, Tang S, Liu H, Fan J, Zhang F, Farina EM, Mohammed MK, Zou Y, Song D, Liao J, Huang J, Guo D, Lu M, Liu F, Liu J, Li L, Ma C, Hu X, Haydon RC, Lee MJ, Reid RR, Ameer GA, Yang L, He TC. A thermoresponsive polydiolcitrate-gelatin scaffold and delivery system mediates effective bone formation from BMP9-transduced mesenchymal stem cells. Biomed Mater. 2016 Apr 21; 11(2):025021. PMID: 27097687.
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    32. Lu S, Wu J, Xu S, Fu B, Dong J, Yang Y, Wang G, Xin M, Li Q, He TC, Wang F, Zhou D. Medial approach to treat humeral mid-shaft fractures: a retrospective study. J Orthop Surg Res. 2016 Mar 17; 11:32. PMID: 26988227.
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    33. Denduluri SK, Scott B, Lamplot JD, Yin L, Yan Z, Wang Z, Ye J, Wang J, Wei Q, Mohammed MK, Haydon RC, Kang RW, He TC, Athiviraham A, Ho SH, Shi LL. Immortalized Mouse Achilles Tenocytes Demonstrate Long-Term Proliferative Capacity While Retaining Tenogenic Properties. Tissue Eng Part C Methods. 2016 Mar; 22(3):280-9. PMID: 26959762.
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    34. Lu S, Wu J, Fu B, Dong J, Yang Y, Xin M, Wang G, He TC, Zhou D. Transiliac Osteotomy in Surgical Management of Pelvic Post-Traumatic Malunions: A Retrospective Study. Medicine (Baltimore). 2016 Mar; 95(13):e3144. PMID: 27043674.
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    35. Wang J, Wei Q, Wang X, Tang S, Liu H, Zhang F, Mohammed MK, Huang J, Guo D, Lu M, Liu F, Liu J, Ma C, Hu X, Haydon RC, He TC, Luu HH. Transition to resistance: An unexpected role of the EMT in cancer chemoresistance. Genes Dis. 2016 Mar; 3(1):3-6. PMID: 28491932.
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    36. Mohammed MK, Shao C, Wang J, Wei Q, Wang X, Collier Z, Tang S, Liu H, Zhang F, Huang J, Guo D, Lu M, Liu F, Liu J, Ma C, Shi LL, Athiviraham A, He TC, Lee MJ. Wnt/ß-catenin signaling plays an ever-expanding role in stem cell self-renewal, tumorigenesis and cancer chemoresistance. Genes Dis. 2016 Mar; 3(1):11-40. PMID: 27077077.
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    37. Xie Y, Huang S, He T, Su Y. Coffee consumption and risk of gastric cancer: an updated meta-analysis. Asia Pac J Clin Nutr. 2016; 25(3):578-88. PMID: 27440694.
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    38. Wang CZ, Anderson S, DU W, He TC, Yuan CS. Red ginseng and cancer treatment. Chin J Nat Med. 2016 Jan; 14(1):7-16. PMID: 26850342.
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    39. Li Y, Wagner ER, Yan Z, Wang Z, Luther G, Jiang W, Ye J, Wei Q, Wang J, Zhao L, Lu S, Wang X, Mohammed MK, Tang S, Liu H, Fan J, Zhang F, Zou Y, Song D, Liao J, Haydon RC, Luu HH, He TC. The Calcium-Binding Protein S100A6 Accelerates Human Osteosarcoma Growth by Promoting Cell Proliferation and Inhibiting Osteogenic Differentiation. Cell Physiol Biochem. 2015; 37(6):2375-92. PMID: 26646427.
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    40. Deng Y, Zhang J, Wang Z, Yan Z, Qiao M, Ye J, Wei Q, Wang J, Wang X, Zhao L, Lu S, Tang S, Mohammed MK, Liu H, Fan J, Zhang F, Zou Y, Liao J, Qi H, Haydon RC, Luu HH, He TC, Tang L. Antibiotic monensin synergizes with EGFR inhibitors and oxaliplatin to suppress the proliferation of human ovarian cancer cells. Sci Rep. 2015 Dec 07; 5:17523. PMID: 26639992.
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    41. Yang K, Wang X, Zhang H, Wang Z, Nan G, Li Y, Zhang F, Mohammed MK, Haydon RC, Luu HH, Bi Y, He TC. The evolving roles of canonical WNT signaling in stem cells and tumorigenesis: implications in targeted cancer therapies. Lab Invest. 2016 Feb; 96(2):116-36. PMID: 26618721.
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    42. Yuan SM, Li H, Yang M, Zha H, Sun H, Li XR, Li AF, Gu Y, Duan L, Luo JY, Li CY, Wang Y, Wang ZB, He TC, Zhou L. High intensity focused ultrasound enhances anti-tumor immunity by inhibiting the negative regulatory effect of miR-134 on CD86 in a murine melanoma model. Oncotarget. 2015 Nov 10; 6(35):37626-37. PMID: 26485753.
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    43. Green JD, Tollemar V, Dougherty M, Yan Z, Yin L, Ye J, Collier Z, Mohammed MK, Haydon RC, Luu HH, Kang R, Lee MJ, Ho SH, He TC, Shi LL, Athiviraham A. Multifaceted signaling regulators of chondrogenesis: Implications in cartilage regeneration and tissue engineering. Genes Dis. 2015 Dec; 2(4):307-327. PMID: 26835506.
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    192. Luu HH, Song WX, Luo X, Manning D, Luo J, Deng ZL, Sharff KA, Montag AG, Haydon RC, He TC. Distinct roles of bone morphogenetic proteins in osteogenic differentiation of mesenchymal stem cells. J Orthop Res. 2007 May; 25(5):665-77. PMID: 17290432.
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    193. Luo Q, Kang Q, Song WX, Luu HH, Luo X, An N, Luo J, Deng ZL, Jiang W, Yin H, Chen J, Sharff KA, Tang N, Bennett E, Haydon RC, He TC. Selection and validation of optimal siRNA target sites for RNAi-mediated gene silencing. Gene. 2007 Jun 15; 395(1-2):160-9. PMID: 17449199.
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    194. Luo J, Chen J, Deng ZL, Luo X, Song WX, Sharff KA, Tang N, Haydon RC, Luu HH, He TC. Wnt signaling and human diseases: what are the therapeutic implications? Lab Invest. 2007 Feb; 87(2):97-103. PMID: 17211410.
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    195. Haydon RC, Luu HH, He TC. Osteosarcoma and osteoblastic differentiation: a new perspective on oncogenesis. Clin Orthop Relat Res. 2007 Jan; 454:237-46. PMID: 17075380.
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    196. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, Sharff KA, Luu HH, Haydon RC, Kinzler KW, Vogelstein B, He TC. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc. 2007; 2(5):1236-47. PMID: 17546019.
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    197. Wang CZ, Zhang B, Song WX, Wang A, Ni M, Luo X, Aung HH, Xie JT, Tong R, He TC, Yuan CS. Steamed American ginseng berry: ginsenoside analyses and anticancer activities. J Agric Food Chem. 2006 Dec 27; 54(26):9936-42. PMID: 17177524.
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    198. Wang CZ, Luo X, Zhang B, Song WX, Ni M, Mehendale S, Xie JT, Aung HH, He TC, Yuan CS. Notoginseng enhances anti-cancer effect of 5-fluorouracil on human colorectal cancer cells. Cancer Chemother Pharmacol. 2007 Jun; 60(1):69-79. PMID: 17009031.
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    199. Zhang BQ, Huang Y, Tang N, Wu Y, Zhang J, Chen WX, He TC, Huang AL. [Inhibition of HBV replication and antigen expression by RNA interference against different targets]. Zhonghua Gan Zang Bing Za Zhi. 2006 Sep; 14(9):662-5. PMID: 16995979.
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    200. Zhang Y, An HS, Thonar EJ, Chubinskaya S, He TC, Phillips FM. Comparative effects of bone morphogenetic proteins and sox9 overexpression on extracellular matrix metabolism of bovine nucleus pulposus cells. Spine (Phila Pa 1976). 2006 Sep 01; 31(19):2173-9. PMID: 16946650.
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    201. Si W, Kang Q, Luu HH, Park JK, Luo Q, Song WX, Jiang W, Luo X, Li X, Yin H, Montag AG, Haydon RC, He TC. CCN1/Cyr61 is regulated by the canonical Wnt signal and plays an important role in Wnt3A-induced osteoblast differentiation of mesenchymal stem cells. Mol Cell Biol. 2006 Apr; 26(8):2955-64. PMID: 16581771.
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    202. Zhang Y, Li Z, Thonar EJ, An HS, He TC, Pietryla D, Phillips FM. Transduced bovine articular chondrocytes affect the metabolism of cocultured nucleus pulposus cells in vitro: implications for chondrocyte transplantation into the intervertebral disc. Spine (Phila Pa 1976). 2005 Dec 01; 30(23):2601-7. PMID: 16319745.
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    203. Luu HH, Zhou L, Haydon RC, Deyrup AT, Montag AG, Huo D, Heck R, Heizmann CW, Peabody TD, Simon MA, He TC. Increased expression of S100A6 is associated with decreased metastasis and inhibition of cell migration and anchorage independent growth in human osteosarcoma. Cancer Lett. 2005 Nov 08; 229(1):135-48. PMID: 16157226.
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    204. Phillips FM, Bolt PM, He TC, Haydon RC. Gene therapy for spinal fusion. Spine J. 2005 Nov-Dec; 5(6 Suppl):250S-258S. PMID: 16291120.
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    205. He TC. Distinct osteogenic activity of BMPs and their orthopaedic applications. J Musculoskelet Neuronal Interact. 2005 Oct-Dec; 5(4):363-6. PMID: 16340140.
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    206. Tao P, Zhang J, Tang N, Zhang BQ, He TC, Huang AL. Potent and specific inhibition of SARS-CoV antigen expression by RNA interference. Chin Med J (Engl). 2005 May 05; 118(9):714-9. PMID: 15899131.
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    207. Luo J, Sun MH, Kang Q, Peng Y, Jiang W, Luu HH, Luo Q, Park JY, Li Y, Haydon RC, He TC. Gene therapy for bone regeneration. Curr Gene Ther. 2005 Apr; 5(2):167-79. PMID: 15853725.
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    208. Sun J, Hobert ME, Duan Y, Rao AS, He TC, Chang EB, Madara JL. Crosstalk between NF-kappaB and beta-catenin pathways in bacterial-colonized intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2005 Jul; 289(1):G129-37. PMID: 15790758.
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    209. Akintola-Ogunremi O, Luo Q, He TC, Wang HL. Is cytomegalovirus associated with human colorectal tumorigenesis? Am J Clin Pathol. 2005 Feb; 123(2):244-9. PMID: 15842049.
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    210. Luu HH, Kang Q, Park JK, Si W, Luo Q, Jiang W, Yin H, Montag AG, Simon MA, Peabody TD, Haydon RC, Rinker-Schaeffer CW, He TC. An orthotopic model of human osteosarcoma growth and spontaneous pulmonary metastasis. Clin Exp Metastasis. 2005; 22(4):319-29. PMID: 16170668.
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    211. Mehta V, Kang Q, Luo J, He TC, Haydon RC, Mass DP. Characterization of adenovirus-mediated gene transfer in rabbit flexor tendons. J Hand Surg Am. 2005 Jan; 30(1):136-41. PMID: 15680569.
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    212. Luu HH, Zhang R, Haydon RC, Rayburn E, Kang Q, Si W, Park JK, Wang H, Peng Y, Jiang W, He TC. Wnt/beta-catenin signaling pathway as a novel cancer drug target. Curr Cancer Drug Targets. 2004 Dec; 4(8):653-71. PMID: 15578921.
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    213. Luo Q, Kang Q, Si W, Jiang W, Park JK, Peng Y, Li X, Luu HH, Luo J, Montag AG, Haydon RC, He TC. Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J Biol Chem. 2004 Dec 31; 279(53):55958-68. PMID: 15496414.
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    214. Peng Y, Kang Q, Luo Q, Jiang W, Si W, Liu BA, Luu HH, Park JK, Li X, Luo J, Montag AG, Haydon RC, He TC. Inhibitor of DNA binding/differentiation helix-loop-helix proteins mediate bone morphogenetic protein-induced osteoblast differentiation of mesenchymal stem cells. J Biol Chem. 2004 Jul 30; 279(31):32941-9. PMID: 15161906.
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    215. He TC. Adenoviral vectors. Curr Protoc Hum Genet. 2004 May; Chapter 12:Unit 12.4. PMID: 18428355.
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    216. Haydon RC, Zhou L, He TC. Tyrosine kinase inhibitor STI-571: the new wonder drug of cancer therapy. Cancer Biol Ther. 2004 Apr; 3(4):393-4. PMID: 15004535.
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    217. Park JY, Luo Q, Jiang W, Kang Q, Peng Y, Strom C, Luu HH, Haydon RC, He TC. Dual regulation of gene expression mediated by tetracycline and Cre recombinase. Biotechniques. 2004 Mar; 36(3):390-2, 394, 396. PMID: 15038152.
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    218. Peng Y, Kang Q, Cheng H, Li X, Sun MH, Jiang W, Luu HH, Park JY, Haydon RC, He TC. Transcriptional characterization of bone morphogenetic proteins (BMPs)-mediated osteogenic signaling. J Cell Biochem. 2003 Dec 15; 90(6):1149-65. PMID: 14635189.
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    219. Deyrup AT, Haydon RC, Huo D, Ishikawa A, Peabody TD, He TC, Montag AG. Myoid differentiation and prognosis in adult pleomorphic sarcomas of the extremity: an analysis of 92 cases. Cancer. 2003 Aug 15; 98(4):805-13. PMID: 12910526.
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    220. Tang N, Huang AL, Zhang BQ, Yan G, He TC. [Potent and specific inhibition of hepatitis B virus antigen expression by RNA interference]. Zhonghua Yi Xue Za Zhi. 2003 Aug 10; 83(15):1309-12. PMID: 12930684.
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    221. Cheng H, Jiang W, Phillips FM, Haydon RC, Peng Y, Zhou L, Luu HH, An N, Breyer B, Vanichakarn P, Szatkowski JP, Park JY, He TC. Osteogenic activity of the fourteen types of human bone morphogenetic proteins (BMPs). J Bone Joint Surg Am. 2003 Aug; 85-A(8):1544-52. PMID: 12925636.
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    222. Xiang MQ, Huang AL, Tang N, Xiao YJ, Yan G, He TC. [The expression of Recombinant adenovirus IkappaBalphaM in human hepatocarcinoma HepG2 and it's inhibitive effect to the activity of NF-kappaB]. Zhonghua Yi Xue Za Zhi. 2003 Jul 10; 83(13):1156-60. PMID: 12921635.
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    223. Zhou L, An N, Haydon RC, Zhou Q, Cheng H, Peng Y, Jiang W, Luu HH, Vanichakarn P, Szatkowski JP, Park JY, Breyer B, He TC. Tyrosine kinase inhibitor STI-571/Gleevec down-regulates the beta-catenin signaling activity. Cancer Lett. 2003 Apr 25; 193(2):161-70. PMID: 12706873.
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    224. Paul R, Haydon RC, Cheng H, Ishikawa A, Nenadovich N, Jiang W, Zhou L, Breyer B, Feng T, Gupta P, He TC, Phillips FM. Potential use of Sox9 gene therapy for intervertebral degenerative disc disease. Spine (Phila Pa 1976). 2003 Apr 15; 28(8):755-63. PMID: 12698117.
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    225. Haydon RC, Deyrup A, Ishikawa A, Heck R, Jiang W, Zhou L, Feng T, King D, Cheng H, Breyer B, Peabody T, Simon MA, Montag AG, He TC. Cytoplasmic and/or nuclear accumulation of the beta-catenin protein is a frequent event in human osteosarcoma. Int J Cancer. 2002 Dec 01; 102(4):338-42. PMID: 12402302.
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    226. Wang HL, Wang J, Xiao SY, Haydon R, Stoiber D, He TC, Bissonnette M, Hart J. Elevated protein expression of cyclin D1 and Fra-1 but decreased expression of c-Myc in human colorectal adenocarcinomas overexpressing beta-catenin. Int J Cancer. 2002 Oct 01; 101(4):301-10. PMID: 12209953.
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    227. Haydon RC, Zhou L, Feng T, Breyer B, Cheng H, Jiang W, Ishikawa A, Peabody T, Montag A, Simon MA, He TC. Nuclear receptor agonists as potential differentiation therapy agents for human osteosarcoma. Clin Cancer Res. 2002 May; 8(5):1288-94. PMID: 12006550.
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    228. Shih IM, Yu J, He TC, Vogelstein B, Kinzler KW. The beta-catenin binding domain of adenomatous polyposis coli is sufficient for tumor suppression. Cancer Res. 2000 Mar 15; 60(6):1671-6. PMID: 10749138.
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    229. He TC, Chan TA, Vogelstein B, Kinzler KW. PPARdelta is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell. 1999 Oct 29; 99(3):335-45. PMID: 10555149; PMCID: PMC3779681.
    230. da Costa LT, He TC, Yu J, Sparks AB, Morin PJ, Polyak K, Laken S, Vogelstein B, Kinzler KW. CDX2 is mutated in a colorectal cancer with normal APC/beta-catenin signaling. Oncogene. 1999 Sep 02; 18(35):5010-4. PMID: 10490837.
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    231. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science. 1998 Sep 04; 281(5382):1509-12. PMID: 9727977.
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    232. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A. 1998 Mar 03; 95(5):2509-14. PMID: 9482916; PMCID: PMC19394.
    233. Hermeking H, Lengauer C, Polyak K, He TC, Zhang L, Thiagalingam S, Kinzler KW, Vogelstein B. 14-3-3sigma is a p53-regulated inhibitor of G2/M progression. Mol Cell. 1997 Dec; 1(1):3-11. PMID: 9659898.
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    234. Polyak K, Waldman T, He TC, Kinzler KW, Vogelstein B. Genetic determinants of p53-induced apoptosis and growth arrest. Genes Dev. 1996 Aug 01; 10(15):1945-52. PMID: 8756351.
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    235. Jiang N, He TC, Miyajima A, Wojchowski DM. The box1 domain of the erythropoietin receptor specifies Janus kinase 2 activation and functions mitogenically within an interleukin 2 beta-receptor chimera. J Biol Chem. 1996 Jul 12; 271(28):16472-6. PMID: 8663338.
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    236. Da Costa LT, Jen J, He TC, Chan TA, Kinzler KW, Vogelstein B. Converting cancer genes into killer genes. Proc Natl Acad Sci U S A. 1996 Apr 30; 93(9):4192-6. PMID: 8633039; PMCID: PMC39510.
    237. Zhuang H, Niu Z, He TC, Patel SV, Wojchowski DM. Erythropoietin-dependent inhibition of apoptosis is supported by carboxyl-truncated receptor forms and blocked by dominant-negative forms of Jak2. J Biol Chem. 1995 Jun 16; 270(24):14500-4. PMID: 7782312.
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    238. He TC, Jiang N, Zhuang H, Wojchowski DM. Erythropoietin-induced recruitment of Shc via a receptor phosphotyrosine-independent, Jak2-associated pathway. J Biol Chem. 1995 May 12; 270(19):11055-61. PMID: 7538110.
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    239. Zhuang H, Patel SV, He TC, Niu Z, Wojchowski DM. Dominant negative effects of a carboxy-truncated Jak2 mutant on Epo-induced proliferation and Jak2 activation. Biochem Biophys Res Commun. 1994 Oct 14; 204(1):278-83. PMID: 7945371.
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    240. Zhuang H, Patel SV, He TC, Sonsteby SK, Niu Z, Wojchowski DM. Inhibition of erythropoietin-induced mitogenesis by a kinase-deficient form of Jak2. J Biol Chem. 1994 Aug 26; 269(34):21411-4. PMID: 8063772.
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    241. He TC, Jiang N, Zhuang H, Quelle DE, Wojchowski DM. The extended box 2 subdomain of erythropoietin receptor is nonessential for Jak2 activation yet critical for efficient mitogenesis in FDC-ER cells. J Biol Chem. 1994 Jul 15; 269(28):18291-4. PMID: 8034573.
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    242. He TC, Zhuang H, Jiang N, Waterfield MD, Wojchowski DM. Association of the p85 regulatory subunit of phosphatidylinositol 3-kinase with an essential erythropoietin receptor subdomain. Blood. 1993 Dec 15; 82(12):3530-8. PMID: 7505116.
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    243. Wojchowski DM, He TC. Signal transduction in the erythropoietin receptor system. Stem Cells. 1993 Sep; 11(5):381-92. PMID: 8241949.
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