Hypoxia Regulates CD44 and Its Variant Isoforms through HIF-1α in Triple Negative Breast Cancer

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Krishnamachary, Balaji ^a   Penet, Marie France ^a   Nimmagadda, Sridhar ^a   Mironchik, Yelena ^a   Raman, Venu ^a,b   Solaiyappan, Meiyappan ^a   Semenza, Gregg L ^a,b   Pomper, Martin G ^a,b   Bhujwalla, Zaver M ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD44V ANTIGEN; CD44V6 ANTIGEN; CD44V7 ANTIGEN; CD44V8 ANTIGEN; HERMES ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IODINE 125; MESSENGER RNA; MONOCLONAL ANTIBODY; RED FLUORESCENT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CANCER CELL CULTURE; CELL COUNT; CELL SURFACE; CONTROLLED STUDY; EXON; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC ENGINEERING; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HYPOXIA; IN VIVO STUDY; ISOTOPE LABELING; MOUSE; NONHUMAN; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TRIPLE NEGATIVE BREAST CANCER; TUMOR XENOGRAFT;

ANOXIA; ANTIGENS, CD44; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; PROTEIN ISOFORMS;

EID: 84865507272     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044078     Document Type: Article

References (40)

1. Vaupel P, Mayer A, (2007) Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 26: 225-239.
2. Semenza GL, (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732.
3. Moeller BJ, Dewhirst MW, (2006) HIF-1 and tumour radiosensitivity. Br J Cancer 95: 1-5.
4. Jubb AM, Buffa FM, Harris AL, (2010) Assessment of tumour hypoxia for prediction of response to therapy and cancer prognosis. J Cell Mol Med 14: 18-29.
5. Krishnamachary B, Berg-Dixon S, Kelly B, Agani F, Feldser D, et al. (2003) Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res 63: 1138-1143.
6. Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, et al. (1999) Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res 59: 5830-5835.
7. Peng ST, Su CH, Kuo CC, Shaw CF, Wang HS, (2007) CD44 crosslinking-mediated matrix metalloproteinase-9 relocation in breast tumor cells leads to enhanced metastasis. Int J Oncol 31: 1119-1126.
8. Gotte M, Yip GW, (2006) Heparanase, hyaluronan, and CD44 in cancers: a breast carcinoma perspective. Cancer Res 66: 10233-10237.
9. Fukazawa H, Yoshida K, Ichinohasama R, Sawai T, Hiromatsu Y, et al. (1993) Expression of the Hermes-1 (CD44) and ICAM-1 (CD54) molecule on the surface of thyroid cells from patients with Graves' disease. Thyroid: official journal of the American Thyroid Association 3: 285-289.
10. Khan SA, Cook AC, Kappil M, Gunthert U, Chambers AF, et al. (2005) Enhanced cell surface CD44 variant (v6, v9) expression by osteopontin in breast cancer epithelial cells facilitates tumor cell migration: novel post-transcriptional, post-translational regulation. Clin Exp Metastasis 22: 663-673.
11. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, et al. (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100: 672-679.
12. Dontu G, Al-Hajj M, Abdallah WM, Clarke MF, Wicha MS, (2003) Stem cells in normal breast development and breast cancer. Cell Prolif 36Suppl 1: 59-72.
13. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF, (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988.
14. Panchision DM, (2009) The role of oxygen in regulating neural stem cells in development and disease. J Cell Physiol 220: 562-568.
15. Ceradini DJ, Gurtner GC, (2005) Homing to hypoxia: HIF-1 as a mediator of progenitor cell recruitment to injured tissue. Trends Cardiovasc Med 15: 57-63.
16. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE, (2006) Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 12: 1167-1174.
17. Hoffmeyer MR, Wall KM, Dharmawardhane SF, (2005) In vitro analysis of the invasive phenotype of SUM 149, an inflammatory breast cancer cell line. Cancer Cell Int 5: 11.
18. van Golen KL, Davies S, Wu ZF, Wang Y, Bucana CD, et al. (1999) A novel putative low-affinity insulin-like growth factor-binding protein, LIBC (lost in inflammatory breast cancer), and RhoC GTPase correlate with the inflammatory breast cancer phenotype. Clin Cancer Res 5: 2511-2519.
19. Raman V, Artemov D, Pathak AP, Winnard PT Jr, McNutt S, et al. (2006) Characterizing vascular parameters in hypoxic regions: a combined magnetic resonance and optical imaging study of a human prostate cancer model. Cancer Res 66: 9929-9936.
20. Krishnamachary B, Glunde K, Wildes F, Mori N, Takagi T, et al. (2009) Noninvasive detection of lentiviral-mediated choline kinase targeting in a human breast cancer xenograft. Cancer Res 69: 3464-3471.
21. Krishnamachary B, Zagzag D, Nagasawa H, Rainey K, Okuyama H, et al. (2006) Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B. Cancer Res 66: 2725-2731.
22. Fraker PJ, Speck JC Jr, (1978) Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a,6a-diphrenylglycoluril. Biochem Biophys Res Commun 80: 849-857.
23. Giatromanolaki A, Sivridis E, Fiska A, Koukourakis MI, (2011) The CD44+/CD24- phenotype relates to 'triple-negative' state and unfavorable prognosis in breast cancer patients. Medical oncology 28: 745-752.
24. Fillmore CM, Kuperwasser C, (2008) Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 10: R25.
25. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, et al. (2006) CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 8: R59.
26. Avigdor A, Goichberg P, Shivtiel S, Dar A, Peled A, et al. (2004) CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood 103: 2981-2919.
27. Nervi B, Link DC, DiPersio JF, (2006) Cytokines and hematopoietic stem cell mobilization. J Cell Biochem 99: 690-705.
28. Louie E, Nik S, Chen JS, Schmidt M, Song B, et al. (2010) Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation. Breast Cancer Res 12: R94.
29. Doyle LA, Ross DD, (2003) Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene 22: 7340-7358.
30. Das B, Tsuchida R, Malkin D, Koren G, Baruchel S, et al. (2008) Hypoxia Enhances Tumor Stemness by Increasing the Invasive and Tumorigenic Side-Population Fraction. Stem Cells 26: 1818-1830.
31. Krishnamurthy P, Ross DD, Nakanishi T, Bailey-Dell K, Zhou S, et al. (2004) The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 279: 24218-24225.
32. Klingbeil P, Marhaba R, Jung T, Kirmse R, Ludwig T, et al. (2009) CD44 variant isoforms promote metastasis formation by a tumor cell-matrix cross-talk that supports adhesion and apoptosis resistance. Mol Cancer Res 7: 168-179.
33. Kopp R, Fichter M, Schalhorn G, Danescu J, Classen S, (2009) Frequent expression of the high molecular, 673-bp CD44v3,v8-10 variant in colorectal adenomas and carcinomas. Int J Mol Med 24: 677-683.
34. Diaz LK, Zhou X, Wright ET, Cristofanilli M, Smith T, et al. (2005) CD44 expression is associated with increased survival in node-negative invasive breast carcinoma. Clin Cancer Res 11: 3309-3314.
35. Berner HS, Suo Z, Risberg B, Villman K, Karlsson MG, et al. (2003) Clinicopathological associations of CD44 mRNA and protein expression in primary breast carcinomas. Histopathology 42: 546-554.
36. Jung T, Castellana D, Klingbeil P, Hernandez IC, Vitacolonna M, et al. (2009) CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 11: 1093-1105.
37. Bourguignon LY, Wong G, Earle C, Krueger K, Spevak CC, (2010) Hyaluronan-CD44 interaction promotes c-Src-mediated twist signaling, microRNA-10b expression, and RhoA/RhoC up-regulation, leading to Rho-kinase-associated cytoskeleton activation and breast tumor cell invasion. J Biol Chem 285: 36721-36735.
38. Jothy S, (2003) CD44 and its partners in metastasis. Clin Exp Metastasis 20: 195-201.
39. Gao F, Okunieff P, Han Z, Ding I, Wang L, et al. (2005) Hypoxia-induced alterations in hyaluronan and hyaluronidase. Advances in experimental medicine and biology 566: 249-256.
40. Turcotte S, Desrosiers RR, Beliveau R, (2004) Hypoxia upregulates von Hippel-Lindau tumor-suppressor protein through RhoA-dependent activity in renal cell carcinoma. American journal of physiology Renal physiology 286: F338-348.