Osteoblast-secreted collagen upregulates paracrine Sonic hedgehog signaling by prostate cancer cells and enhances osteoblast differentiation

Molecular Cancer

Volumn 11, Issue , 2012, Pages

  Zunich, Samantha M ^a   Valdovinos, Maria ^a   Douglas, Taneka ^a   Walterhouse, David ^a   Iannaccone, Philip ^a   Lamm, Marilyn L G ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Bone metastasis; Collagen; Extracellular matrix; Hedgehog; Osteoblast differentiation; Prostate cancer

Indexed keywords

ALKALINE PHOSPHATASE; ASCORBIC ACID; COLLAGEN; PROTEIN PATCHED 1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; FIBRILLAR COLLAGEN;

ARTICLE; CANCER CELL CULTURE; CELL DIFFERENTIATION; CELL INTERACTION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; OSTEOBLAST; PARACRINE SIGNALING; PROSTATE CANCER; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CHEMISTRY; COCULTURE; CYTOCHEMISTRY; CYTOLOGY; DRUG EFFECT; MALE; METABOLISM; MOUSE; PARTICLE SIZE; PATHOLOGY; PHYSIOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

ERINACEIDAE;

ALKALINE PHOSPHATASE; ANIMALS; ASCORBIC ACID; CELL DIFFERENTIATION; CELL LINE, TUMOR; COCULTURE TECHNIQUES; FIBRILLAR COLLAGENS; HEDGEHOG PROTEINS; HISTOCYTOCHEMISTRY; HUMANS; MALE; MICE; OSTEOBLASTS; PARACRINE COMMUNICATION; PARTICLE SIZE; PROSTATIC NEOPLASMS; UP-REGULATION;

EID: 84860509714     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-11-30     Document Type: Article

References (43)

1. Bubendorf L, Schöpfer A, Wagner U, Sauter G, Moch H, Willi N, Gasser TC, Mihatsch MJ. Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 2000, 31:578-583. 10.1053/hp.2000.6698, 10836297.
2. Greenlee RT, Hill-Harmon MB, Murray T, Thun M. Cancer statistics, 2001. CA Cancer J Clin 2001, 51:15-36. 10.3322/canjclin.51.1.15, 11577478.
3. Keller ET, Zhang J, Cooper CR, Smith PC, McCauley LK, Pienta KJ, Taichman RS. Prostate carcinoma skeletal metastases: cross-talk between tumor and bone. Cancer Metastasis Rev 2001, 20:333-349. 10.1023/A:1015599831232, 12085970.
4. Bussard KM, Gay CV, Mastro AM. The bone microenvironment in metastasis; what is special about bone?. Cancer Metastasis Rev 2008, 27:41-55. 10.1007/s10555-007-9109-4, 18071636.
5. Josson S, Matsuoka Y, Chung LWK, Zhau HE, Wang R. Tumor-stroma co-evolution in prostate cancer progression and metastasis. Semin Cell Dev Biol 2010, 21:26-32. 10.1016/j.semcdb.2009.11.016, 3388105, 19948237.
6. Zunich SM, Douglas T, Valdovinos M, Chang T, Bushman W, Walterhouse D, Iannaccone P, Lamm MLG. Paracrine sonic hedgehog signaling by prostate cancer cells induces osteoblast differentiation. Mol Cancer 2009, 8:12-22. 10.1186/1476-4598-8-12, 2654862, 19254376.
7. Cohen MM. The hedgehog signaling network. Am J Med Genet 2003, 123A:5-28. 10.1002/ajmg.a.20495, 14556242.
8. Lamm MLG, Bushman W. Hedgehog signalling in prostate morphogenesis. In Shh and Gli Signalling and Development 2006, 116-124. Landes Bioscience, Austin and Springer, New York, Fisher CE, Howie SEM.
9. Iannaccone P, Holmgren R, Lamm MLG, Ahlgren S, Lakiza O, Yoon JW, Walterhouse D. The sonic hedgehog signaling pathway. In Inborn Errors of Development 2008, 263-279. Oxford University Press, Epstein CJ, Erickson RP, Wynshaw-Boris A, 2.
10. Fan L, Pepicelli CV, Dibble CC, Catbagan W, Zarycki JL, Laciak R, Gipp J, Shaw A, Lamm MLG, Munoz A, Lipinski R, Thrasher JB, Bushman W. Hedgehog signaling promotes prostate xenograft tumor growth. Endocrinology 2004, 145:3961-3970. 10.1210/en.2004-0079, 15132968.
11. Karhadkar SS, Bova GS, Abdallah N, Dhara S, Gardner D, Maitra A, Issacs JT, Berman DM, Beachy PA. Hedgehog signaling in prostate regeneration, neoplasia and metastasis. Nature 2004, 431:707-711. 10.1038/nature02962, 15361885.
12. Sanchez P, Hernández AM, Stecca B, Kahler AJ, DeGueme AM, Barrett A, Beyna M, Datta MW, Datta S, Ruiz i Altaba A. Inhibition of prostate cancer proliferation by interference with SONIC-HEDGEHOG-GLI1 signaling. Proc Natl Acad Sci U S A 2004, 101:12561-12566. 10.1073/pnas.0404956101, 514658, 15314219.
13. Sheng T, Li C, Zhang X, Chi S, He N, Chen K, McCormick F, Gatalica Z, Xie J. Activation of the hedgehog pathway in advanced prostate cancer. Mol Cancer 2004, 3:29-41. 10.1186/1476-4598-3-29, 524523, 15482598.
14. Quarles LD, Yohay DA, Lever LW, Caton R, Wenstrup RJ. Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development. J Bone Miner Res 1992, 7:683-692.
15. Franceschi RT. The developmental control of osteoblast-specific gene expression: role of specific transcription factors and the extracellular matrix environment. Crit Rev Oral Biol Med 1999, 10:40-57. 10.1177/10454411990100010201, 10759426.
16. Franceschi RT, Iyer BS. Relationship between collagen synthesis and expression of the osteoblast phenotype in MC3T3-E1 cells. J Bone Miner Res 1992, 7:235-246.
17. Aronow MA, Gerstenfeld LC, Owen TA, Tassinari MS, Stein GS, Lian JB. Factors that promote progressive development of the osteoblast phenotype in cultured fetal rat calvaria cells. J Cell Physiol 1990, 143:213-221. 10.1002/jcp.1041430203, 2332447.
18. Franceschi RT, Iyer BS, Cui Y. Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3-E1 cells. J Bone Miner Res 1994, 9:843-854.
19. Murad S, Grove D, Lindberg KA, Reynolds G, Sivarajah A, Pinnell SR. Regulation of collagen synthesis by ascorbic acid. Proc Natl Acad Sci U S A 1981, 78:2879-2882. 10.1073/pnas.78.5.2879, 319462, 6265920.
20. Starborg T, Lu Y, Kadler KE, Holmes DF. Electron microscopy of collagen fibril structure in vitro and in vivo including three dimensional reconstruction. In: Methods in Cell Biology Vol 2008, 88:319-345.
21. Rosenblatt M. Remarks on some nonparametric estimates of a density function. Annals Mathematical Statistics 1956, 27:832-837.
22. Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M. Overexpression of lysyl hydroxylase-2b leads to defective collagen fibrillogenesis and matrix mineralization. J Bone Miner Res 2005, 20:81-87. 10.1359/JBMR.041026, 15619673.
23. Blissett AR, Garbellini D, Calomeni EP, Mihai C, Elton TS, Agarwal G. Regulation of collagen fibrillogenesis by cell-surface expression of kinase dead DDR2. J Mol Biol 2009, 385:902-911. 10.1016/j.jmb.2008.10.060, 2677101, 18996394.
24. Uitto J, Prockop DJ. Incorporation of proline analogs into collagen polypeptides. Effect on the production of extracellular procollagen and on the stability of the triple helical structure of the molecule. Biochim Biophys Acta 1974, 336:234-251.
25. Gullberg D, Gehlsen KR, Turner DC, Ahlén K, Zijenah LS, Barnes MJ, Rubin K. Analysis of alpha 1 beta 1, alpha 2 beta 1 and alpha 3 beta 1 integrins in cell-collagen interactions: identification of conformation dependent alpha 1 beta 1 binding sites in collagen type I. EMBO J 1992, 11:3865-3873. 556896, 1396580.
26. Longhurst CM, Jennings LK. Integrin-mediated signal transduction. Cell Mol Life Sci 1998, 54:514-526. 10.1007/s000180050180, 9676571.
27. Miranti CK, Brugge JS. Sensing the environment: a historical perspective on integrin signal transduction. Nat Cell Biol 2002, 4:E83-90. 10.1038/ncb0402-e83, 11944041.
28. Lauth M, Toftgård R. Non-canonical activation of GLI transcription factors: implications for targeted anti-cancer therapy. Cell Cycle 2007, 6:2458-2463. 10.4161/cc.6.20.4808, 17726373.
29. Goel HL, Underwood JM, Nickerson JA, Hsieh CC, Languino LR. Beta1 integrins mediate cell proliferation in three-dimensional cultures by regulating expression of the sonic hedgehog effector protein, GLI1. J Cell Physiol 2010, 224:210-217. 2885855, 20333644.
30. Takeuchi Y, Nakayama K, Matsumoto T. Differentiation and cell surface expression of transforming growth factor-beta receptors are regulated by interaction with matrix collagen in murine osteoblastic cells. J Biol Chem 1996, 271:3938-3944. 10.1074/jbc.271.7.3938, 8632016.
31. Torii Y, Hitomi K, Tsukagoshi N. Synergistic effect of BMP-2 and ascorbate on the phenotypic expression of osteoblastic MC3T3-E1 cells. Mol Cell Biochem 1996, 165:25-29.
32. Suzawa M, Takeuchi Y, Fukumoto S, Kato S, Ueno N, Miyazono K, Matsumoto T, Fujita T. Extracellular matrix-associated bone morphogenetic proteins are essential for differentiation of murine osteoblastic cells in vitro. Endocrinology 1999, 140:2125-2133. 10.1210/en.140.5.2125, 10218963.
33. Pons S, Martí E. Sonic hedgehog synergizes with the extracellular matrix protein vitronectin to induce spinal motor neuron differentiation. Development 2000, 127:333-342.
34. Blaess S, Graus-Porta D, Belvindrah R, Radakovits R, Pons S, Littlewood-Evans A, Senften M, Guo H, Li Y, Miner JH, Reichardt LF, Müller U. Beta1-integrins are critical for cerebellar granule cell precursor proliferation. J Neurosci 2004, 24:3402-3412. 10.1523/JNEUROSCI.5241-03.2004, 2693074, 15056720.
35. Otsuka E, Yamaguchi A, Hirose S, Hagiwara H. Characterization of osteoblastic differentiation of stromal cell line ST2 that is induced by ascorbic acid. Am J Physiol Cell Physiol 1999, 277:C132-C138.
36. Leon ER, Iwasaki K, Komaki M, Kojima T, Ishikawa I. Osteogenic effect of interleukin-11 and synergism with ascorbic acid in human periodontal ligament cells. J Periodont Res 2007, 42:527-535. 10.1111/j.1600-0765.2007.00977.x, 17956465.
37. Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med 2006, 4:38-52. 10.1186/1741-7015-4-38, 1781458, 17190588.
38. Wang W, Wyckoff JB, Frohlich VC, Oleynikov Y, Hüttelmaier S, Zavadil J, Cermak L, Bottinger EP, Singer RH, White JG, Segall JE, Condeelis JS. Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res 2002, 62:6278-6288.
39. Ezura Y, Chakravarti S, Oldberg A, Chervoneva I, Birk DE. Differential expression of lumican and fibromodulin regulate collagen fibrillogenesis in developing mouse tendons. J Cell Biol 2000, 151:779-787. 10.1083/jcb.151.4.779, 2169450, 11076963.
40. Young BB, Gordon MK, Birk DE. Expression of type XIV collagen in developing chicken tendons: association with assembly and growth of collagen fibrils. Dev Dyn 2000, 217:430-439. 10.1002/(SICI)1097-0177(200004)217:4<430::AID-DVDY10>3.0.CO;2-5, 10767087.
41. Shaw A, Gipp J, Bushman W. The Sonic Hedgehog pathway stimulates prostate tumor growth by paracrine signaling and recapitulates embryonic gene expression in tumor myofibroblasts. Oncogene 2009, 28:4480-4490. 10.1038/onc.2009.294, 2795794, 19784071.
42. Maramag C, Menon M, Balaji KC, Reddy PG, Laxmanan S. Effect of vitamin C on prostate cancer cells in vitro: effect on cell number, viability, and DNA synthesis. Prostate 1997, 32:188-195. 10.1002/(SICI)1097-0045(19970801)32:3<188::AID-PROS5>3.0.CO;2-H, 9254898.
43. Frömberg A, Gutsch D, Schulze D, Vollbracht C, Weiss G, Czubayko F, Aigner A. Ascorbate exerts anti-proliferative effects through cell cycle inhibition and sensitizes tumor cells towards cytostatic drugs. Cancer Chemother Pharmacol 2011, 67:1157-1166. 10.1007/s00280-010-1418-6, 3082037, 20694726.