Deletion of the SPARC acidic domain or EGF-like module reduces SPARC-induced migration and signaling through p38 MAPK/HSP27 in glioma

Carcinogenesis

Volumn 33, Issue 2, 2012, Pages 275-284

  McClung, Heather M ^a,b   Golembieski, William A ^a   Schultz, Chad R ^a   Jankowski, Michelle ^a   Schultz, Lonni R ^a   Rempel, Sandra A ^a,b  

^a HENRY FORD HOSPITAL   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 27; HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; OSTEONECTIN;

ARTICLE; CELL MIGRATION; CELL SURFACE; DELETION MUTANT; GLIOMA; HUMAN; HUMAN CELL; IMAGING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN STABILITY; WESTERN BLOTTING;

EID: 84856573441     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgr276     Document Type: Article

References (55)

1. Rempel, S.A. et al(2006) Tumor invasiveness and anti-invasion strategies. In Newton, H.B. (ed.) Handbook of Brain Tumor Chemotherapy. Elsevier Inc., San Diego, CA, pp. 193-218.
2. Lefranc, F. et al(2005) Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J. Clin. Oncol., 23, 2411-2422.
3. Louis, D.N(2006) Molecular pathology of malignant gliomas. Annu. Rev. Pathol., 1, 97-117.
4. Demuth, T. et al(2004) Molecular mechanisms of glioma cell migration and invasion. J. Neurooncol., 70, 217-228.
5. Sage, H. et al(1984) Characterization of a novel serum albumin-binding glycoprotein secreted by endothelial cells in culture. J. Biol. Chem., 259, 3993-4007.
6. Termine, J.D. et al(1981) Osteonectin, a bone-specific protein linking mineral to collagen. Cell, 26, 99-105.
7. Mann, K. et al(1987) Solubilization of protein BM-40 from a basement membrane tumor with chelating agents and evidence for its identity with osteonectin and SPARC. FEBS. Lett., 218, 167-172.
8. Lane, T.F. et al(1994) The biology of SPARC, a protein that modulates cell-matrix interactions. FASEB J., 8, 163-173.
9. Sage, E.H(1997) Terms of attachment: SPARC and tumorigenesis. Nat. Med., 3, 144-146.
10. Framson, P.E. et al(2004) SPARC and tumor growth: where the seed meets the soil? J. Cell. Biochem., 92, 679-690.
11. Rempel, S.A. et al(1998) SPARC: a signal of astrocytic neoplastic transformation and reactive response in human primary and xenograft gliomas. J. Neuropathol. Exp. Neurol., 57, 1112-1121.
12. Golembieski, W.A. et al(1999) Increased SPARC expression promotes U87 glioblastoma invasion in vitro. Int. J. Dev. Neurosci., 17, 463-472.
13. Schultz, C. et al(2002) Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res., 62, 6270-6277.
14. Rich, J.N. et al(2003) Bone-related genes expressed in advanced malignancies induce invasion and metastasis in a genetically defined human cancer model. J. Biol. Chem., 278, 15951-15957.
15. Maurer, P. et al(1992) High-affinity and low-affinity calcium binding and stability of the multidomain extracellular 40-kDa basement membrane glycoprotein (BM-40/SPARC/osteonectin). Eur. J. Biochem., 205, 233-240.
16. Hohenester, E. et al(1997) Crystal structure of a pair of follistatin-like and EF-hand calcium-binding domains in BM-40. EMBO J., 16, 3778-3786.
17. Weaver, M.S. et al(2008) The copper binding domain of SPARC mediates cell survival in vitro via interaction with integrin beta1 and activation of integrin-linked kinase. J. Biol. Chem., 283, 22826-22837.
18. Hohenester, E. et al(1996) Structure of a novel extracellular Ca(2{thorn})-binding module in BM-40. Nat. Struct. Biol., 3, 67-73.
19. Busch, E. et al(2000) Calcium affinity, cooperativity, and domain interactions of extracellular EF-hands present in BM-40. J. Biol. Chem., 275, 25508-25515.
20. Lane, T.F. et al(1990) Functional mapping of SPARC: peptides from two distinct Ca+(+)-binding sites modulate cell shape. J. Cell. Biol., 111, 3065-3076.
21. Murphy-Ullrich, J.E. et al(1995) SPARC mediates focal adhesion disassembly in endothelial cells through a follistatin-like region and the Ca(2+)-binding EF-hand. J. Cell. Biochem., 57, 341-350.
22. Lane, T.F. et al(1992) Regulation of gene expression by SPARC during angiogenesis in vitro. Changes in fibronectin, thrombospondin-1, and plasminogen activator inhibitor-1. J. Biol. Chem., 267, 16736-16745.
23. Funk, S.E. et al(1991) The Ca2(+)-binding glycoprotein SPARC modulates cell cycle progression in bovine aortic endothelial cells. Proc. Natl. Acad. Sci. USA, 88, 2648-2652.
24. Funk, S.E. et al(1993) Differential effects of SPARC and cationic SPARC peptides on DNA synthesis by endothelial cells and fibroblasts. J. Cell. Physiol., 154, 53-63.
25. Yost, J.C. et al(1993) Specific interaction of SPARC with endothelial cells is mediated through a carboxyl-terminal sequence containing a calciumbinding EF hand. J. Biol. Chem., 268, 25790-25796.
26. Chlenski, A. et al(2004) Neuroblastoma angiogenesis is inhibited with a folded synthetic molecule corresponding to the epidermal growth factor-like module of the follistatin domain of SPARC. Cancer Res., 64, 7420-7425.
27. Motamed, K. et al(1998) SPARC inhibits endothelial cell adhesion but not proliferation through a tyrosine phosphorylation-dependent pathway. J. Cell. Biochem., 70, 543-552.
28. Mayer, U. et al(1991) Calcium-dependent binding of basement membrane protein BM-40 (osteonectin, SPARC) to basement membrane collagen type IV. Eur. J. Biochem., 198, 141-150.
29. Golembieski, W.A. et al(2008) HSP27 mediates SPARC-induced changes in glioma morphology, migration, and invasion. Glia, 56, 1061-1075.
30. Nie, J. et al(2008) IFATS collection: combinatorial peptides identify alpha5beta1 integrin as a receptor for the matricellular protein SPARC on adipose stromal cells. Stem Cells, 26, 2735-2745.
31. Thomas, S.L. et al(2010) PTEN augments SPARC suppression of proliferation and inhibits SPARC-induced migration by suppressing SHC-RAFERK and AKT signaling. Neuro Oncol., 12, 941-955.
32. Shi, Q. et al(2007) Targeting SPARC expression decreases glioma cellular survival and invasion associated with reduced activities of FAK and ILK kinases. Oncogene, 26, 4084-4094.
33. Barker, T.H. et al(2005) SPARC regulates extracellular matrix organization through its modulation of integrin-linked kinase activity. J. Biol. Chem., 280, 36483-36493.
34. Esfandiarei, M. et al(2010) Integrin-linked kinase functions as a downstream signal of platelet-derived growth factor to regulate actin polymerization and vascular smooth muscle cell migration. BMC Cell Biol., 11, 16.
35. Guay, J. et al(1997) Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J. Cell Sci., 110, (Pt 3), 357-368.
36. Rane, M.J. et al(2001) p38 Kinase-dependent MAPKAPK-2 activation functions as 3-phosphoinositide-dependent kinase-2 for Akt in human neutrophils. J. Biol. Chem., 276, 3517-3523.
37. Wu, R. et al(2007) Hsp27 regulates Akt activation and polymorphonuclear leukocyte apoptosis by scaffolding MK2 to Akt signal complex. J. Biol. Chem., 282, 21598-21608.
38. Zheng, C. et al(2006) MAPK-activated protein kinase-2 (MK2)-mediated formation and phosphorylation-regulated dissociation of the signal complex consisting of p38, MK2, Akt, and Hsp27. J. Biol. Chem., 281, 37215-37226.
39. Schafer, C. et al(1999) HSP27 expression regulates CCK-induced changes of the actin cytoskeleton in CHO-CCK-A cells. Am. J. Physiol., 277, C1032-C1043.
40. Emerson, R.O. et al(2006) Chaperone-like activity revealed in the matricellular protein SPARC. J. Cell. Biochem., 98, 701-705.
41. Martinek, N. et al(2007) Is SPARC an evolutionarily conserved collagen chaperone? J. Dent. Res., 86, 296-305.
42. Nomura, N. et al(2007) Phorbol 12-myristate 13-acetate (PMA)-induced cell migration of glioblastoma cells is mediated via p38 MAPK/HSP27 pathway. Biochem. Pharmacol., 74, 690-701.
43. Mimnaugh, E.G. et al(2004) Simultaneous inhibition of hsp 90 and the proteasome promotes protein ubiquitination, causes endoplasmic reticulum-derived cytosolic vacuolization, and enhances antitumor activity. Mol. Cancer Ther., 3, 551-566.
44. Mason, I.J. et al(1986) Evidence from molecular cloning that SPARC, a major product of mouse embryo parietal endoderm, is related to an endothelial cell 'culture shock' glycoprotein of Mr 43,000. EMBO J., 5, 1465-1472.
45. Gooden, M.D. et al(1999) Cell cycle-dependent nuclear location of the matricellular protein SPARC: association with the nuclear matrix. J. Cell. Biochem., 74, 152-167.
46. Kzhyshkowska, J. et al(2008) Alternatively activated macrophages regulate extracellular levels of the hormone placental lactogen via receptormediated uptake and transcytosis. J. Immunol., 180, 3028-3037.
47. Zhang, J. et al(2009) A novel GGA-binding site is required for intracellular sorting mediated by stabilin-1. Mol. Cell. Biol., 29, 6097-6105.
48. Rempel, S.A. et al(2001) SPARC modulates cell growth, attachment and migration of U87 glioma cells on brain extracellular matrix proteins. J. Neurooncol., 53, 149-160.
49. Maglott, A. et al(2006) The small alpha5beta1 integrin antagonist, SJ749, reduces proliferation and clonogenicity of human astrocytoma cells. Cancer Res., 66, 6002-6007.
50. Mahesparan, R. et al(2003) Expression of extracellular matrix components in a highly infiltrative in vivo glioma model. Acta. Neuropathol., 105, 49-57.
51. Ohnishi, T. et al(1998) Role of fibronectin-stimulated tumor cell migration in glioma invasion in vivo: clinical significance of fibronectin and fibronectin receptor expressed in human glioma tissues. Clin. Exp. Metastasis, 16, 729-741.
52. Beadle, C. et al(2008) The role of myosin II in glioma invasion of the brain. Mol. Biol. Cell, 19, 3357-3368.
53. Pichon, S. et al(2004) Control of actin dynamics by p38 MAP kinase-Hsp27 distribution in the lamellipodium of smooth muscle cells. J. Cell Sci., 117, 2569-2577.
54. Atorrasagasti, C. et al(2010) Overexpression of SPARC obliterates the in vivo tumorigenicity of human hepatocellular carcinoma cells. Int. J. Cancer, 126, 2726-2740.
55. Chlenski, A. et al(2010) Modulation of matrix remodeling by SPARC in neoplastic progression. Semin. Cell Dev. Biol., 21, 55-65.