The pathology of tumor stromatogenesis

Cancer Biology and Therapy

Volumn 6, Issue 5, 2007, Pages 639-645

  Giatromanolaki, Alexandra ^a   Sivridis, Efthimios ^a   Koukourakis, Michael I ^a  

^a DEMOCRITUS UNIVERSITY OF THRACE MEDICAL SCHOOL   (Greece)

Author keywords

Invasion; Metastasis; Neostroma; Stromagenesis; Stromatogenesis; Tumor metabolism

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; OSTEONECTIN; PLATELET DERIVED GROWTH FACTOR RECEPTOR; THYMIDINE PHOSPHORYLASE;

CANCER INVASION; CELL ACTIVATION; CELL INVASION; CELL METABOLISM; CELL PROLIFERATION; ENDOTHELIUM CELL; FIBROBLAST; MYOFIBROBLAST; PROTEIN EXPRESSION; REVIEW; SPINDLE CELL; STROMA CELL; TUMOR CELL; TUMOR GROWTH; ANIMAL; CARCINOGENESIS; HUMAN; METABOLISM; NEOPLASM; PATHOLOGY; TUMOR INVASION; ULTRASTRUCTURE;

ANIMALS; CARCINOGENESIS; FIBROBLASTS; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; STROMAL CELLS;

EID: 34548256761     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.6.5.4198     Document Type: Review

References (105)

1. Weiss L. Biomechanical interactions of cancer cells with the microvasculature during hematogenous metastasis. Cancer Metastasis Rev 1992; 11:227-35.
2. Saini A. Cell adhesion molecules in cancer. In: Vile RG, ed. Cancer Metastasis: From Mechanisms to Therapies. Chichester: John Wiley and Sons, 1995:71-98.
3. Stoker M, Gherardi E. Regulation of cell movement: The motogenic cytokines. Biochim Biophys Acta 1991; 1072:88-102.
4. Rosen EM, Knesel J, Goldberg ID. Scatter factor and its relationship to hepatocyte growth factor and met. Cell Growth Differ 1991; 2:603-7.
5. Vile RG. Invasion in cancer metastasis - The journey from the primary tumour to the circulation. In: Vile RG, ed. Cancer Metastasis: From Mechanisms to Therapies. Chichester: John Wiley and Sons, 1995:21-46.
6. Strauli P, Haemmerli O. The role of cancer cell motility in invasion. Canner Metastasis Rev 184; 3:127-131.
7. Enterline HT, Coman DR. The amoeboid motility of human and animal neoplastic cells. Cancer 1950; 3:1033-8.
8. Mohler JL, Partin AW, Coffey DS. Prediction of metastatic potential by a new grading system of cell motility: Validation in the Dunning R-3327 prostatic adenocarcinoma model. J Urol 1987; 138:168-70.
9. Liotta LA, Steeg PS, Stetler-Stevenson WG. Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation. Cell 1991; 64:327-36.
10. Aznavoorian S, Murphy A, Stetler-Stevenson WG. Molecular aspects of tumour cell invasion and metastasis. Cancer 1993; 71:1368-1383.
11. Basset P, Bellocq JP, Wolf C. A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinoma. Nature 1990; 348:699-704.
12. Sivridis E, Giatromanolaki A, Koukourakis MI. The vascular network of tumours - What is it not for? J Pathol 2003; 201:173-80.
13. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol 2002; 29(Suppl 16):15-8.
14. Sivridis E, Giatromanolaki A, Koukourakis MI. "Stromatogenesis" and tumour progression. Int J Surg Pathol 2004; 12:1-9.
15. Sivridis E, Giatromanolaki A, Koukourakis MI. Proliferating fibroblasts at the invading tumour edge of colorectal adenocarcinomas are associated with endogenous markers of hypoxia, acidity, and oxidative stress. J Clin Pathol 2005; 58:1033-8.
16. Giatromanolaki A, Sivridis E, Koukourakis MI. Tumour angiogenesis: Vascular growth and survival. APMIS 2004; 112:431-440.
17. Sivridis E, Giatromanolaki A, Galazios G, Koukourakis MI. Node-related factors and survival in node-positive breast carcinomas. Breast 2005; 15:382-9.
18. Koukourakis MI, Giatromanolaki A, Harris AL, Sivridis E. Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: A metabolic survival role for tumor-associated stroma. Cancer Res 2006; 66:632-7.
19. Redler P, Lustig ES. Differences in the growth-promoting effect of normal and peritumoral dermis on epidermis in vitro. Dev Biol 1968; 17:679-91.
20. Dawe CJ, Morgan WD, Slatick MS. Influence of epithelio-mesenchymal interactions on tumor induction by polyoma virus. Int J Cancer 1966; 1:419-50.
21. Bissell MJ, Radisky DC, Rizki A, Weaver VM, Petersen OW. The organizing principle: Microenvironmental influences in the normal and malignant breast. Differentiation 2002; 70:537-46.
22. Willhauck MJ, Mirancea N, Vosseler S, Pavesio A, Boukamp P, Mueller MM, Fusenig NE, Stark HJ. Reversion of tumor phenotype in surface transplants of skin SCC cells by scaffold-induced stroma modulation. Carcinogenesis 2006.
23. Cunha GR, Hayward SW, Wang YZ, Ricke WA. Role of the stromal microenvironment in carcinogenesis of the prostate. Int J Cancer 2003; 107:1-10.
24. Thompson TC, Timme TL, Kadmon D, Park SH, Egawa S, Yoshida K. Genetic predisposition and mesenchymal-epithelial interactions in ras+myc-induced carcinogenesis in reconstituted mouse prostate. Mol Carcinog 1993; 7:165-79.
25. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, Shappell S, Washington MK, Neilson EG, Moses HL. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004; 303:848-51.
26. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 1999; 59:5002-11.
27. Shekhar MP, Werdell J, Santner SJ, Pauley RJ, Tait L. Breast stroma plays a dominant regulatory role in breast epithelial growth and differentiation: Implications for tumor development and progression. Cancer Res 2001; 61:1320-6.
28. Camps JL, Chang SM, Hsu TC, Freeman MR, Hong SJ, Zhau HE, von Eschenbach AC, Chung LW. Fibroblast-mediated acceleration of human epithelial tumor growth in vivo. Proc Natl Acad Sci USA 1990; 87:75-9.
29. Kitadai Y, Sasaki T, Kuwai T, Nakamura T, Bucana CD, Hamilton SR, Fidler IJ. Expression of activated platelet-derived growth factor receptor in stromal cells of human colon carcinomas is associated with metastatic potential. Int J Cancer 2006; 119:2567-74.
30. Cekanova M, Masi T, Plummer IIIrd HK, Majidi M, Fedorocko P, Schuller HM. Pulmonary fibroblasts stimulate the proliferation of cell lines from human lung adenocarcinomas. Anticancer Drugs 2006; 17:771-81.
31. Cat B, Stuhlmann D, Steinbrenner H, Alili L, Holtkotter O, Sies H, Brenneisen P. Enhancement of tumor invasion depends on transdifferentiation of skin fibroblasts mediated by reactive oxygen species. J Cell Sci 2006; 119:2727-38.
32. Hasebe T, Tsuda H, Tsubono Y, Imoto S, Mukai K. Fibrotic focus in invasive ductal carcinoma of the breast: A histopathological prognostic parameter for tumor recurrence and tumor death within three years after the initial operation. Jpn Cancer Res 1997; 88:590-599.
33. Ruiter D, Bogenrieder T, Elder D, Herlyn M. Melanoma-stroma interactions: Structural and functional aspects. Lancet Oncol 2002; 3:35-43.
34. Koukourakis MI, Giatromanolaki A, Brekken RA, Sivridis E, Gatter KC, Harris AL, Sage EH. Enhanced expression of SPARC/osteonectin in the tumor-associated stroma of non-small cell lung cancer is correlated with markers of hypoxia/acidity and with poor prognosis of patients. Cancer Res 2003; 63:5376-80.
35. Koukourakis MI, Giatromanolaki A, Kakolyris S, O'Byrne KJ, Apostolikas N, Skarlatos J, Gatter KC, Harris AL. Different patterns of stromal and cancer cell thymidine phosphorylase reactivity in non-small-cell lung cancer: Impact on tumour neoangiogenesis and survival. Br J Cancer. 1998; 77:1696-703.
36. Sivridis E, Giatromanolaki A, Anastasiadis P, Georgiou L, Gatter KC, Harris AL, Bicknell R, Koukourakis MI. Tumour and angiogenesis research group: Angiogenic co-operation of VEGF and stromal cell TP in endometrial carcinomas. J Pathol 2002; 196:416-22.
37. Sivridis E, Giatromanolaki A, Koukourakis MI. Proliferating fibroblasts at the invading tumour edge of colorectal adenocarcinomas are associated with endogenous markers of hypoxia, acidity, and oxidative stress. J Clin Pathol 2005; 58:1033-8.
38. Fromigue O, Louis K, Dayem M, Milanini J, Pages G, Tartare-Deckert S, Ponzio G, Hofman P, Barbry P, Auberger P, Mari B. Gene expression profiling of normal human pulmonary fibroblasts following coculture with non-small-cell lung cancer cells reveals alterations related to matrix degradation, angiogenesis, cell growth and survival. Oncogene 2003; 22:8487-8497.
39. Nakagawa H, Liyanarachchi S, Davuluri RV, Auer H, Martin Jr EW, de la Chapelle A, Frankel WL. Role of cancer-associated stromal fibroblasts in metastatic colon cancer to the liver and their expression profiles. Oncogene 2004; 23:366-7377.
40. Liu Y, Kalen A, Risto O, Wahlstrom O. Fibroblast proliferation due to exposure to a platelet concentrate in vitro is pH dependent. Wound Repair Regen 2002; 10:336-340.
41. Wong YC, Tam NN. Dedifferentiation of stromal smooth muscle as a factor in prostate carcinogenesis. Differentiation 2002; 70:633-45.
42. Schurch W, Seemayer TA, Gabbiani G. Myofibroblast. In: Sternberg SS, ed. Histology for Pathologists. New York: Raven Press, 1992:109-144.
43. Lagace R, Grimaud JA, Shurch W, Seemayeer TA. Myofibroblastic stromal reaction in carcinomas of the breast and variations of collagenous matrix and structural glycoproteins. Virchows Arch 1985; 408:49-59.
44. Longacre TA, Hendrickson MR. Diffusely infiltrative endometrial adenocarcinoma: An adenoma malignum pattern of myoinvasion. Am J Surg Pathol 1999; 23:69-78.
45. Direkze NC, Hodivala-Dilke K, Jeffery R, Hunt T, Poulsom R, Oukrif D, Alison MR, Wright NA. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res 2004; 64:8492-5.
46. Cheng JD, Dunbrack Jr RL, Valianou M, Rogatko A, Alpaugh RK, Weiner LM. Promotion of tumor growth by murine fibroblast activation protein, a serine protease, in an animal model. Cancer Res 2002; 62:4767-72.
47. Cheng JD, Valianou M, Canutescu AA, Jaffe EK, Lee HO, Wang H, Lai JH, Bachovchin WW, Weiner LM. Abrogation of fibroblast activation protein enzymatic activity attenuates tumor growth. Mol Cancer Ther 2005; 4:351-60.
48. Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakakura T. Tenascin: An extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 1986; 47:131-9.
49. Briggs J, Chamboredon S, Castellazzi M, Kerry JA, Bos TJ. Transcriptional upregulation of SPARC, in response to c-Jun overexpression, contributes to increased motility and invasion of MCF7 breast cancer cells. Oncogene 2002; 21:7077-91.
50. Schultz C, Lemke N, Ge S, Golembieski WA, Rempel SA. Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res 2002; 62:6270-7.
51. Takebayashi Y, Akiyama S, Akiba S, Yamada K, Miyadera K, Sumizawa T, Yamada Y, Murata F, Aikou T. Clinicopathologic and prognostic significance of an angiogenic factor, thymidine phosphorylase, in human colorectal carcinoma. J Natl Cancer Inst 1996; 88:1110-7.
52. Giatromanolaki A, Sivridis E, Simopoulos C, Polychronidis A, Gatter KC, Harris AL, Koukourakis MI. Thymidine phosphorylase expression in gallbladder adenocarcinomas. Int J Surg Pathol 2002; 10:181-8.
53. Sivridis E, Giatromanolaki A, Anastasiadis P, Georgiou L, Gatter KC, Harris AL, Bicknell R, Koukourakis MI. Angiogenic co-operation of VEGF and stromal cell TP in endometrial carcinomas. J Pathol 2002; 196:416-22.
54. Brown NS, Jones A, Fujiyama C, Harris AL, Bicknell R. Thymidine phosphorylase induces carcinoma cell oxidative stress and promotes secretion of angiogenic factors. Cancer Res 2000; 60:6298-302.
55. Sengupta S, Sellers LA, Matheson HB, Fan TP. Thymidine phosphorylase induces angiogenesis in vivo and in vitro: An evaluation of possible mechanisms. Br J Pharmacol 2003; 139:219-31.
56. Giatromanolaki A, Sivridis E, Kouskoukis C, Gatter KC, Harris AL, Koukourakis MI. Hypoxia-inducible factors 1alpha and 2alpha are related to vascular endothelial growth factor expression and a poorer prognosis in nodular malignant melanomas of the skin. Melanoma Res 2003; 13:493-501.
57. Sivridis E, Giatromanolaki A, Koukourakis MI, Bicknell R, Harris AL, Gatter KC. Thymidine phosphorylase expression in endometrial carcinomas. Clin Exp Metastasis 1999; 17:445-50.
58. Sivridis E, Giatromanolaki A, Papadopoulos I, Gatter KC, Harris AL, Koukourakis MI. Thymidine phosphorylase expression in normal, hyperplastic and neoplastic prostates: Correlation with tumour associated macrophages, infiltrating lymphocytes, and angiogenesis. Br J Cancer 2002; 86:1465-71.
59. Toi M, Inada K, Hoshina S, Suzuki H, Kondo S, Tominaga T. Vascular endothelial growth factor and platelet-derived endothelial cell growth factor are frequently coexpressed in highly vascularized human breast cancer. Clin Cancer Res 1995; 1:961-964.
60. Koukourakis MI, Giatromanolaki A, O'Byrne KJ, Comley M, Whitehouse RM, Talbot DC, Gatter KC, Harris AL. Platelet-derived endothelial cell growth factor expression correlates with tumour angiogenesis and prognosis in non-small-cell lung cancer. Br J Cancer 1997; 75:477-81.
61. Giatromanolaki A, Koukourakis MI, Sivridis E, Turley H, Talks K, Pezzella F, Gatter KC, Harris AL. Relation of hypoxia inducible factor 1 alpha and 2 alpha in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival. Br J Cancer 2001; 85:881-90.
62. Koukourakis MI, Giatromanolaki A, Fountzilas G, Sivridis E, Gatter KC, Harris AL. Angiogenesis, thymidine phosphorylase, and resistance of squamous cell head and neck cancer to cytotoxic and radiation therapy. Clin Cancer Res 2000; 6:381-9.
63. Gabbiani G, Lelous M, Bailey AJ, Bazin S, Delauney A. Collagen and myofibroblasts of granulation tissue. Virchows Archiv [Cell Pathol] 1976; 21:133-145.
64. D'Ardenne AJ. Ground substance. In: McGee JO'D, Isaacson PG, Wright NA, eds. Oxford Textbook of Pathology: Principles of Pathology. Vol 1. Oxford: Oxford Umiversity Press, 1992:58-63.
65. Lynch CC, Matrisian LM. Matrix metalloproteinases in tumor-host cell communication. Differentiation 2002; 70:561-73.
66. Nelson AR, Fingleton B, Rothenberg ML, Matrisian LM. Matrix metalloproteinases: Biologic activity and clinical implications. J Clin Oncol 2000; 18:1135-49.
67. Schuler T, Kornig S, Blankenstein T. Tumor rejection by modulation of tumor stromal fibroblasts. J Exp Med 2003; 198:1487-93.
68. Furuhashi M, Sjoblom T, Abramsson A, Ellingsen J, Micke P, Li H, Bergsten-Folestad E, Eriksson U, Heuchel R, Betsholtz C, Heldin CH, Ostman A. Platelet-derived growth factor production by B16 melanoma cells leads to increased pericyte abundance in tumors and an associated increase in tumor growth rate. Cancer Res 2004; 64:2725-33.
69. Ishii G, Sangai T, Sugiyama K, Ito T, Hasebe T, Endoh Y, Magae J, Ochiai A. In vivo characterization of bone marrow-derived fibroblasts recruited into fibrotic lesions. Stem Cells 2005; 23:699-706.
70. Sangai T, Ishii G, Kodama K, Miyamoto S, Aoyagi Y, Ito T, Magae J, Sasaki H, Nagashima T, Miyazaki M, Ochiai A. Effect of differences in cancer cells and tumor growth sites on recruiting bone marrow-derived endothelial cells and myofibroblasts in cancer-induced stroma. Int J Cancer 2005; 115:885-92.
71. Vaughan MB, Howard EW, Tomasek JJ. Transforming growth factor-beta1 promotes the morphological and functional differentiation of the myofibroblast. Exp Cell Res 2000; 257:180-9.
72. Lieubeau B, Garrigue L, Barbieux I, Meflah K, Gregoire M. The role of transforming growth factor beta 1 in the fibroblastic reaction associated with rat colorectal tumor development. Cancer Res 1994; 54:6526-32.
73. Dalal BI, Keown PA, Greenberg AH. Immunocytochemical localization of secreted transforming growth factor-beta 1 to the advancing edges of primary tumors and to lymph node metastases of human mammary carcinoma. Am J Pathol 1993; 143:381-9.
74. Finlay GA, Thannickal VJ, Fanburg BL, Paulson KE. Transforming growth factor-beta 1-induced activation of the ERK pathway/activator protein-1 in human lung fibroblasts requires the autocrine induction of basic fibroblast growth factor. J Biol Chem 2000; 275:27650-6.
75. Yu J, Moon A, Kim HR. Both platelet-derived growth factor receptor (PDGFR)-alpha and PDGFR-beta promote murine fibroblast cell migration. Biochem Biophys Res Commun 2001; 282:697-700.
76. Shao ZM, Nhuyen M, Barsky SH. Human breast carcinoma desmoplasia is PDGF initiated. Oncogene 2000; 19:4337-45.
77. Pertovaara L, Kaipainen A, Mustonen T, Orpana A, Ferrara N, Saksela O, Alitalo K. Vascular endothelial growth factor is induced in response to transforming growth factor-beta in fibroblastic and epithelial cells. J Biol Chem 1994; 269:6271-4.
78. Koukourakis MI, Giatromanolaki A, Thorpe PE, Brekken RA, Sivridis E, Kakolyris S, Georgoulias V, Gatter KC, Harris AL. Vascular endothelial growth factor/KDR activated microvessel density versus CD31 standard microvessel density in non-small cell lung cancer. Cancer Res 2000; 60:3088-95.
79. Moodley YP, Misso NL, Scaffidi AK, Fogel-Petrovic M, McAnulty RJ, Laurent GJ, Thompson PJ, Knight DA. Inverse effects of interleukin-6 on apoptosis of fibroblasts from pulmonary fibrosis and normal lungs. Am J Respir Cell Mol Biol 2003; 29:490-8.
80. Piguet PF. Is "tumor necrosis factor" the major effector of pulmonary fibrosis? Eur Cytokine Netw 1990; 1:257-258.
81. Morimoto M, Irimura T. Fibroblast migratory factor derived from mouse colon carcinoma cells: Potential roles of fibronectin in tumor stroma formation. J Cell Biochem 2001; 80:635-646.
82. Tomasini-Johansson BR, Sundberg C, Lindmark G, Gailit JO, Rubin K. Vitronectin in colorectal adenocarcinoma - synthesis by stromal cells in culture. Exp Cell Res 1994; 214:303-12.
83. De Wever O, Mareel M. Role of tissue stroma in cancer cell invasion. J Pathol 2003; 200:429-47.
84. Almholt K, Johnsen M. Stromal cell involvement in cancer. Recent Results Cancer Res 2003; 162:31-42.
85. Mueller MM, Fusenig NE. Tumor-stroma interactions directing phenotype and progression of epithelial skin tumor cells. Differentiation 2002; 70:486-97.
86. Cunha GR, Hayward SW, Wang YZ. Role of stroma in carcinogenesis of the prostate. Differentiation 2002; 70:473-85.
87. Schor SL, Schor AM. Phenotypic and genetic alterations in mammary stroma: Implications for tumour progression. Breast Cancer Res 2001; 3:373-9.
88. Anderson GR, Stoler DL, Scarcello LA. Normal fibroblasts responding to anoxia exhibit features of the malignant phenotype. J Biol Chem 1989; 264:14885-92.
89. Moinfar F, Man YG, Arnould L, Bratthauer GL, Ratschek M, Tavassoli FA. Concurrent and independent genetic alterations in the stromal and epithelial cells of mammary carcinoma: Implications for tumorigenesis. Cancer Res 2000; 60:2562-6.
90. Man Y, Mannion C, Kuhls E, Moinfar F, Bratthauer GL, Albores-Saavedra J, Tavassoli FA. Allelic losses at 3p and 11p are detected in both epithelial and stromal components of cervical small-cell neuroendocrine carcinoma. Appl Immunohistochem Mol Morphol 2001; 9:340-5.
91. Kurose K, Hoshaw-Woodard S, Adeyinka A, Lemeshow S, Watson PH, Eng C. Genetic model of multi-step breast carcinogenesis involving the epithelium and stroma: Clues to tumour-microenvironment interactions. Hum Mol Genet 2001; 10:1907-13.
92. Tuxhorn JA, Ayala GE, Rowley DR. Reactive stroma in prostate cancer progression. J Urol 2001; 166:2472-83.
93. Sugden MC, Holnes MJ. Recent advances in mechanisms regulating glucose oxidation at the level of pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab 2003; 284:855-62.
94. Holbrook JJA, Liljas A, Steindel SJ, Rossman MG. Lactate dehydrogenase. In: Boyer PD ed. The Enzymes. 3rd ed. Vol. XI. NY: Academic Press, 1975:191-292.
95. Koukourakis MI, Giatromanolaki A, Sivridis E. Lactate dehydrogenase isoenzymes 1 and 5: Differential expression by neoplastic and stromal cells in non-small cell lung cancer and other epithelial malignant tumors. Tumour Biol 2003; 24:199-202.
96. Koukourakis MI, Giatromanolaki A, Sivridis E, Gatter KC, Harris AL. Pyruvate dehydrogenase and pyruvate dehydrogenase kinase expression in non small cell lung cancer and tumor-associated stroma. Neoplasia 2005; 7:1-6.
97. Deplanque G, Harris AL. Anti-angiogenic agents: Clinical trial design and therapies in development. Eur J Cancer 2000; 36:1713-24.
98. Fisher JF, Mobashery S. Recent advances in MMP inhibitor design. Cancer Metastasis Rev 2006; 25:115-36.
99. Hurwitz HI, Fehrenbacher L, Hainsworth JD, Heim W, Berlin J, Holmgren E, Hambleton J, Novotny WF, Kabbinavar F. Bevacizumab in combination with fluorouracil and leucovorin: An active regimen for first-line metastatic colorectal cancer. J Clin Oncol 2005; 23:3502-8.
100. Kitadai Y, Sasaki T, Kuwai T, Nakamura T, Bucana CD, Fidler IJ. Targeting the expression of platelet-derived growth factor receptor by reactive stroma inhibits growth and metastasis of human colon carcinoma. I. Am J Pathol 2006; 169:2054-65.
101. Loeffler M, Kruger JA, Niethammer AG, Reisfeld RA. Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J Clin Invest 2006; 116:1955-62.
102. Lee J, Fassnacht M, Nair S, Boczkowski D, Gilboa E. Tumor immunotherapy targeting fibroblast activation protein, a product expressed in tumor-associated fibroblasts. Cancer Res 2005; 65:11156-63.
103. Cat B, Stuhlmann D, Steinbrenner H, Alili L, Holtkotter O, Sies H, Brenneisen P. Enhancement of tumor invasion depends on transdifferentiation of skin fibroblasts mediated by reactive oxygen species. J Cell Sci 2006; 119:2727-38.
104. Jackson VN, Halestrap AP. The kinetics, substrate, and inhibitor specificity of the monocarboxylate(lactate) transporter of rat liver cells determined using the fluorescent intracellular pH indicator, 2′,7′-bis(carboxyethyl)-5(6)-carboxyfluorescein. J Biol Chem 1996; 271:861-8.
105. Yu Y, Deck JA, Hunsaker LA, Deck LM, Royer RE, Goldberg E, Vander Jagt DL. Selective active site inhibitors of human lactate dehydrogenases A4, B4, and C4. Biochem Pharmacol 2001; 62:81-9.