Tissue Biomarkers in Renal Cell Carcinoma: Intermediate Endpoints in the Selection of Targeted Agents for RCC

Chapter
First Online:

Abstract

Renal cancer is the seventh leading malignant condition among men and the 12th among women. It has been estimated that approximately 58,000 new cases of kidney cancer occurred in 2010 and that, in the same year, approximately 13,000 people died from this disease in the USA [1].

Keywords

Renal Cell Carcinoma Kidney Cancer Clear Cell Renal Cell Carcinoma CAIX Expression Renal Cell Carcinoma Tissue 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This work was supported by the Dana-Farber/Harvard Cancer Center Kidney Cancer SPORE and by an Award from Istituto Dermopatico dell’Immacolata, Italy, to S.S.

References

  1. 1.
    American Cancer Society (2001) Kidney cancer (Adult): renal cell carcinoma. http://www.cancer.org/Cancer/KidneyCancer/DetailedGuide/kidney-cancer-adult-key-statistics. Accessed 22 June 2011
  2. 2.
    Cohen HT, McGovern FJ (2005) Renal-cell carcinoma. N Engl J Med 353(23):2477–2490PubMedCrossRefGoogle Scholar
  3. 3.
    Rini BI, Campbell SC, Escudier B (2009) Renal cell carcinoma. Lancet 373(9669):1119–1132PubMedCrossRefGoogle Scholar
  4. 4.
    Lopez-Beltran A et al (2009) 2009 update on the classification of renal epithelial tumors in adults. Int J Urol 16(5):432–443PubMedCrossRefGoogle Scholar
  5. 5.
    Linehan WM et al (2010) Molecular diagnosis and therapy of kidney cancer. Annu Rev Med 61:329–343PubMedCrossRefGoogle Scholar
  6. 6.
    Linehan WM, Srinivasan R, Schmidt LS (2010) The genetic basis of kidney cancer: a metabolic disease. Nat Rev Urol 7(5):277–285PubMedCrossRefGoogle Scholar
  7. 7.
    Rosner I et al (2009) The clinical implications of the genetics of renal cell carcinoma. Urol Oncol 27(2):131–136PubMedCrossRefGoogle Scholar
  8. 8.
    Yagoda A, Abi-Rached B, Petrylak D (1995) Chemotherapy for advanced renal-cell carcinoma: 1983–1993. Semin Oncol 22(1):42–60PubMedGoogle Scholar
  9. 9.
    Motzer RJ, Russo P (2000) Systemic therapy for renal cell carcinoma. J Urol 163(2):408–417PubMedCrossRefGoogle Scholar
  10. 10.
    McDermott DF (2009) Immunotherapy of metastatic renal cell carcinoma. Cancer 115(10 suppl):2298–2305PubMedCrossRefGoogle Scholar
  11. 11.
    McDermott DF, Atkins MB (2008) Immunotherapy of metastatic renal cell carcinoma. Cancer J 14(5):320–324PubMedCrossRefGoogle Scholar
  12. 12.
    McDermott DF, Rini BI (2007) Immunotherapy for metastatic renal cell carcinoma. BJU Int 99(5 Pt B):1282–1288PubMedCrossRefGoogle Scholar
  13. 13.
    Ward JE, Stadler WM (2010) Pazopanib in renal cell carcinoma. Clin Cancer Res 16(24):5923–5927PubMedCrossRefGoogle Scholar
  14. 14.
    Rini BI (2009) Vascular endothelial growth factor-targeted therapy in metastatic renal cell carcinoma. Cancer 115(10 suppl):2306–2312PubMedCrossRefGoogle Scholar
  15. 15.
    Kapoor A, Figlin RA (2009) Targeted inhibition of mammalian target of rapamycin for the treatment of advanced renal cell carcinoma. Cancer 115(16):3618–3630PubMedCrossRefGoogle Scholar
  16. 16.
    Cho D et al (2007) The role of mammalian target of rapamycin inhibitors in the treatment of advanced renal cancer. Clin Cancer Res 13(2 Pt 2):758s–763sPubMedCrossRefGoogle Scholar
  17. 17.
    Azim H, Azim HA Jr, Escudier B (2010) Targeting mTOR in cancer: renal cell is just a beginning. Target Oncol 5(4):269–280PubMedCrossRefGoogle Scholar
  18. 18.
    Atkins MB et al (2009) Treatment selection for patients with metastatic renal cell carcinoma. Cancer 115(10 suppl):2327–2333PubMedCrossRefGoogle Scholar
  19. 19.
    Pal SK et al (2010) Breaking through a plateau in renal cell carcinoma therapeutics: development and incorporation of biomarkers. Mol Cancer Ther 9(12):3115–3125PubMedCrossRefGoogle Scholar
  20. 20.
    Rini BI (2009) Metastatic renal cell carcinoma: many treatment options, one patient. J Clin Oncol 27(19):3225–3234PubMedCrossRefGoogle Scholar
  21. 21.
    Latif F et al (1993) Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 260(5112):1317–1320PubMedCrossRefGoogle Scholar
  22. 22.
    Lonser RR et al (2003) von Hippel-Lindau disease. Lancet 361(9374):2059–2067PubMedCrossRefGoogle Scholar
  23. 23.
    Maher ER, Kaelin WG Jr (1997) von Hippel-Lindau disease. Medicine (Baltimore) 76(6):381–391CrossRefGoogle Scholar
  24. 24.
    Kim WY, Kaelin WG (2004) Role of VHL gene mutation in human cancer. J Clin Oncol 22(24):4991–5004PubMedCrossRefGoogle Scholar
  25. 25.
    Kaelin WG Jr (2004) The von Hippel-Lindau tumor suppressor gene and kidney cancer. Clin Cancer Res 10(18 Pt 2):6290S–6295SPubMedCrossRefGoogle Scholar
  26. 26.
    Gnarra JR et al (1994) Mutations of the VHL tumour suppressor gene in renal carcinoma. Nat Genet 7(1):85–90PubMedCrossRefGoogle Scholar
  27. 27.
    Herman JG et al (1994) Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci USA 91(21):9700–9704PubMedCrossRefGoogle Scholar
  28. 28.
    Beroukhim R et al (2009) Patterns of gene expression and copy-number alterations in von-Hippel Lindau disease-associated and sporadic clear cell carcinoma of the kidney. Cancer Res 69(11):4674–4681PubMedCrossRefGoogle Scholar
  29. 29.
    Nickerson ML et al (2008) Improved identification of von Hippel-Lindau gene alterations in clear cell renal tumors. Clin Cancer Res 14(15):4726–4734PubMedCrossRefGoogle Scholar
  30. 30.
    Kaelin WG Jr (2008) The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat Rev Cancer 8(11):865–873PubMedCrossRefGoogle Scholar
  31. 31.
    Kaelin WG Jr (2007) The von hippel-lindau tumor suppressor protein: an update. Methods Enzymol 435:371–383PubMedCrossRefGoogle Scholar
  32. 32.
    Kondo K et al (2002) Comprehensive mutational analysis of the VHL gene in sporadic renal cell carcinoma: relationship to clinicopathological parameters. Genes Chromosomes Cancer 34(1):58–68PubMedCrossRefGoogle Scholar
  33. 33.
    van Houwelingen KP et al (2005) Prevalence of von Hippel-Lindau gene mutations in sporadic renal cell carcinoma: results from The Netherlands cohort study. BMC Cancer 5:57PubMedCrossRefGoogle Scholar
  34. 34.
    Banks RE et al (2006) Genetic and epigenetic analysis of von Hippel-Lindau (VHL) gene alterations and relationship with clinical variables in sporadic renal cancer. Cancer Res 66(4):2000–2011PubMedCrossRefGoogle Scholar
  35. 35.
    Brauch H et al (2000) VHL alterations in human clear cell renal cell carcinoma: association with advanced tumor stage and a novel hot spot mutation. Cancer Res 60(7):1942–1948PubMedGoogle Scholar
  36. 36.
    Choueiri TK et al (2008) von Hippel-Lindau gene status and response to vascular endothelial growth factor targeted therapy for metastatic clear cell renal cell carcinoma. J Urol 180(3):860–865, discussion 865–866PubMedCrossRefGoogle Scholar
  37. 37.
    Gad S et al (2007) Somatic von Hippel-Lindau (VHL) gene analysis and clinical outcome under antiangiogenic treatment in metastatic renal cell carcinoma: preliminary results. Target Oncol 2(1):3–6CrossRefGoogle Scholar
  38. 38.
    Hutson T et al (2008) Biomarker analysis and final efficacy and safety results of a phase II renal cell carcinoma trial with pazopanib (GW786034), a multi-kinase angiogenesis inhibitor. J Clin Oncol 26(suppl):261s, abstract 5046Google Scholar
  39. 39.
    Patard JJ et al (2008) Low CAIX expression and absence of VHL gene mutation are associated with tumor aggressiveness and poor survival of clear cell renal cell carcinoma. Int J Cancer 123(2):395–400PubMedCrossRefGoogle Scholar
  40. 40.
    Makino Y et al (2002) Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor-3alpha locus. J Biol Chem 277(36):32405–32408PubMedCrossRefGoogle Scholar
  41. 41.
    Maynard MA et al (2003) Multiple splice variants of the human HIF-3 alpha locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J Biol Chem 278(13):11032–11040PubMedCrossRefGoogle Scholar
  42. 42.
    Patel P, Chadalavada R, Ishill N (2008) Hypoxia-inducible factor (HIF) 1-alpha and 2-alpha levels in cell lines and human tumor predicts response to sunitinib in renal cell carcinoma (RCC). J Clin Oncol 26(suppl):252s, abstract 5008Google Scholar
  43. 43.
    Kondo K et al (2002) Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 1(3):237–246PubMedCrossRefGoogle Scholar
  44. 44.
    Maranchie JK et al (2002) The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 1(3):247–255PubMedCrossRefGoogle Scholar
  45. 45.
    Kondo K et al (2003) Inhibition of HIF2alpha is sufficient to suppress pVHL-defective tumor growth. PLoS Biol 1(3):E83PubMedCrossRefGoogle Scholar
  46. 46.
    Mandriota SJ et al (2002) HIF activation identifies early lesions in VHL kidneys: evidence for site-specific tumor suppressor function in the nephron. Cancer Cell 1(5):459–468PubMedCrossRefGoogle Scholar
  47. 47.
    Kaelin WG Jr, Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30(4):393–402PubMedCrossRefGoogle Scholar
  48. 48.
    Hu CJ et al (2003) Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 23(24):9361–9374PubMedCrossRefGoogle Scholar
  49. 49.
    Wang V et al (2005) Differential gene up-regulation by hypoxia-inducible factor-1alpha and hypoxia-inducible factor-2alpha in HEK293T cells. Cancer Res 65(8):3299–3306PubMedGoogle Scholar
  50. 50.
    Lum JJ et al (2007) The transcription factor HIF-1alpha plays a critical role in the growth factor-dependent regulation of both aerobic and anaerobic glycolysis. Genes Dev 21(9):1037–1049PubMedCrossRefGoogle Scholar
  51. 51.
    Papandreou I et al (2006) HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 3(3):187–197PubMedCrossRefGoogle Scholar
  52. 52.
    Kim JW et al (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3(3):177–185PubMedCrossRefGoogle Scholar
  53. 53.
    Gunaratnam L et al (2003) Hypoxia inducible factor activates the transforming growth factor-alpha/epidermal growth factor receptor growth stimulatory pathway in VHL(−/−) renal cell carcinoma cells. J Biol Chem 278(45):44966–44974PubMedCrossRefGoogle Scholar
  54. 54.
    Covello KL et al (2006) HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 20(5):557–570PubMedCrossRefGoogle Scholar
  55. 55.
    Bindra RS et al (2002) VHL-mediated hypoxia regulation of cyclin D1 in renal carcinoma cells. Cancer Res 62(11):3014–3019PubMedGoogle Scholar
  56. 56.
    Gordan JD, Thompson CB, Simon MC (2007) HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 12(2):108–113PubMedCrossRefGoogle Scholar
  57. 57.
    Koshiji M et al (2004) HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 23(9):1949–1956PubMedCrossRefGoogle Scholar
  58. 58.
    Gordan JD et al (2008) HIF-alpha effects on c-Myc distinguish two subtypes of sporadic VHL-deficient clear cell renal carcinoma. Cancer Cell 14(6):435–446PubMedCrossRefGoogle Scholar
  59. 59.
    Bui MH et al (2003) Carbonic anhydrase IX is an independent predictor of survival in advanced renal clear cell carcinoma: implications for prognosis and therapy. Clin Cancer Res 9(2):802–811PubMedGoogle Scholar
  60. 60.
    Atkins M et al (2005) Carbonic anhydrase IX expression predicts outcome of interleukin 2 therapy for renal cancer. Clin Cancer Res 11(10):3714–3721PubMedCrossRefGoogle Scholar
  61. 61.
    Dudek AZ et al (2010) Carbonic anhydrase IX expression is associated with improved outcome of high-dose interleukin-2 therapy for metastatic renal cell carcinoma. Anticancer Res 30(3):987–992PubMedGoogle Scholar
  62. 62.
    McDermott D et al (2010) The high-dose aldesleukin (HD IL-2) “SELECT” trial in patients with metastatic renal cell carcinoma (mRCC). J Clin Oncol 28(15s):345s, abstract 4514Google Scholar
  63. 63.
    Choueiri TK et al (2010) Carbonic anhydrase IX and pathological features as predictors of outcome in patients with metastatic clear-cell renal cell carcinoma receiving vascular endothelial growth factor-targeted therapy. BJU Int 106(6):772–778PubMedCrossRefGoogle Scholar
  64. 64.
    Huang D et al (2010) Interleukin-8 mediates resistance to antiangiogenic agent sunitinib in renal cell carcinoma. Cancer Res 70(3):1063–1071PubMedCrossRefGoogle Scholar
  65. 65.
    Zhang L et al (2011) Resistance of renal cell carcinoma to sorafenib is mediated by potentially reversible gene expression. PLoS One 6(4):e19144PubMedCrossRefGoogle Scholar
  66. 66.
    Bhatt RS et al (2010) Renal cancer resistance to antiangiogenic therapy is delayed by restoration of angiostatic signaling. Mol Cancer Ther 9(10):2793–2802PubMedCrossRefGoogle Scholar
  67. 67.
    Schor-Bardach R et al (2009) Does arterial spin-labeling MR imaging-measured tumor perfusion correlate with renal cell cancer response to antiangiogenic therapy in a mouse model? Radiology 251(3):731–742PubMedCrossRefGoogle Scholar
  68. 68.
    Brat DJ, Bellail AC, Van Meir EG (2005) The role of interleukin-8 and its receptors in gliomagenesis and tumoral angiogenesis. Neuro Oncol 7(2):122–133PubMedCrossRefGoogle Scholar
  69. 69.
    Mizukami Y et al (2005) Induction of interleukin-8 preserves the angiogenic response in HIF-1alpha-deficient colon cancer cells. Nat Med 11(9):992–997PubMedGoogle Scholar
  70. 70.
    Koch AE et al (1992) Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 258(5089):1798–1801PubMedCrossRefGoogle Scholar
  71. 71.
    Smith DR et al (1994) Inhibition of interleukin 8 attenuates angiogenesis in bronchogenic carcinoma. J Exp Med 179(5):1409–1415PubMedCrossRefGoogle Scholar
  72. 72.
    Xu CF et al (2011) Pazopanib efficacy in renal cell carcinoma: evidence for predictive genetic markers in angiogenesis-related and exposure-related genes. J Clin Oncol 29(18):2557–2564PubMedCrossRefGoogle Scholar
  73. 73.
    Varela I et al (2011) Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 469(7331):539–542PubMedCrossRefGoogle Scholar
  74. 74.
    Reisman D, Glaros S, Thompson EA (2009) The SWI/SNF complex and cancer. Oncogene 28(14):1653–1668PubMedCrossRefGoogle Scholar
  75. 75.
    Xia W et al (2008) BAF180 is a critical regulator of p21 induction and a tumor suppressor mutated in breast cancer. Cancer Res 68(6):1667–1674PubMedCrossRefGoogle Scholar
  76. 76.
    Burrows AE, Smogorzewska A, Elledge SJ (2010) Polybromo-associated BRG1-associated factor components BRD7 and BAF180 are critical regulators of p53 required for induction of replicative senescence. Proc Natl Acad Sci USA 107(32):14280–14285PubMedCrossRefGoogle Scholar
  77. 77.
    Kenneth NS et al (2009) SWI/SNF regulates the cellular response to hypoxia. J Biol Chem 284(7):4123–4131PubMedCrossRefGoogle Scholar
  78. 78.
    Klatte T et al (2009) Cytogenetic profile predicts prognosis of patients with clear cell renal cell carcinoma. J Clin Oncol 27(5):746–753PubMedCrossRefGoogle Scholar
  79. 79.
    Shen C et al (2011) Genetic and functional studies implicate HIF1alpha as a 14q kidney cancer suppressor gene. Cancer Discov 1(3):222–235PubMedCrossRefGoogle Scholar
  80. 80.
    Gordan JD et al (2007) HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 11(4):335–347PubMedCrossRefGoogle Scholar
  81. 81.
    Raval RR et al (2005) Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol 25(13):5675–5686PubMedCrossRefGoogle Scholar
  82. 82.
    Mitsumori K et al (2002) Chromosome 14q LOH in localized clear cell renal cell carcinoma. J Pathol 198(1):110–114PubMedCrossRefGoogle Scholar
  83. 83.
    Kaku H et al (2004) Positive correlation between allelic loss at chromosome 14q24-31 and poor prognosis of patients with renal cell carcinoma. Urology 64(1):176–181PubMedCrossRefGoogle Scholar
  84. 84.
    Alimov A et al (2004) Loss of 14q31-q32.2 in renal cell carcinoma is associated with high malignancy grade and poor survival. Int J Oncol 25(1):179–185PubMedGoogle Scholar
  85. 85.
    Shaw RJ, Cantley LC (2006) Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 441(7092):424–430PubMedCrossRefGoogle Scholar
  86. 86.
    Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124(3):471–484PubMedCrossRefGoogle Scholar
  87. 87.
    Bhaskar PT, Hay N (2007) The two TORCs and Akt. Dev Cell 12(4):487–502PubMedCrossRefGoogle Scholar
  88. 88.
    Cho D et al (2007) Potential histologic and molecular predictors of response to temsirolimus in patients with advanced renal cell carcinoma. Clin Genitourin Cancer 5(6):379–385PubMedCrossRefGoogle Scholar
  89. 89.
    Hudson CC et al (2002) Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin. Mol Cell Biol 22(20):7004–7014PubMedCrossRefGoogle Scholar
  90. 90.
    Majumder PK et al (2004) mTOR inhibition reverses Akt-dependent prostate intraepithelial neoplasia through regulation of apoptotic and HIF-1-dependent pathways. Nat Med 10(6):594–601PubMedCrossRefGoogle Scholar
  91. 91.
    Figlin RA et al (2009) Analysis of PTEN and HIF-1alpha and correlation with efficacy in patients with advanced renal cell carcinoma treated with temsirolimus versus interferon-alpha. Cancer 115(16):3651–3660PubMedCrossRefGoogle Scholar
  92. 92.
    Diamandis EP (2010) Cancer biomarkers: can we turn recent failures into success? J Natl Cancer Inst 102(19):1462–1467PubMedCrossRefGoogle Scholar
  93. 93.
    Pepe MS et al (2001) Phases of biomarker development for early detection of cancer. J Natl Cancer Inst 93(14):1054–1061PubMedCrossRefGoogle Scholar
  94. 94.
    Ransohoff DF (2007) How to improve reliability and efficiency of research about molecular markers: roles of phases, guidelines, and study design. J Clin Epidemiol 60(12):1205–1219PubMedCrossRefGoogle Scholar
  95. 95.
    Feng Z, Prentice R, Srivastava S (2004) Research issues and strategies for genomic and proteomic biomarker discovery and validation: a statistical perspective. Pharmacogenomics 5(6):709–719PubMedCrossRefGoogle Scholar
  96. 96.
    Goodsaid FM, Mendrick DL (2010) Translational medicine and the value of biomarker qualification. Sci Transl Med 2(47):47ps44PubMedCrossRefGoogle Scholar
  97. 97.
    Sturgeon CM et al (2008) National Academy of Clinical Biochemistry Laboratory Medicine Practice Guidelines for use of tumor markers in clinical practice: quality requirements. Clin Chem 54(8):e1–e10PubMedCrossRefGoogle Scholar
  98. 98.
    Di Napoli A, Signoretti S (2009) Tissue biomarkers in renal cell carcinoma: issues and solutions. Cancer 115(10 suppl):2290–2297PubMedCrossRefGoogle Scholar
  99. 99.
    Signoretti S et al (2008) Tissue-based research in kidney cancer: current challenges and future directions. Clin Cancer Res 14(12):3699–3705PubMedCrossRefGoogle Scholar
  100. 100.
    Baker AF et al (2005) Stability of phosphoprotein as a biological marker of tumor signaling. Clin Cancer Res 11(12):4338–4340PubMedCrossRefGoogle Scholar
  101. 101.
    Bai Y et al (2011) Quantitative assessment shows loss of antigenic epitopes as a function of pre-analytic variables. Lab Invest 91:1253–1261PubMedCrossRefGoogle Scholar
  102. 102.
    Engel KB, Moore HM (2011) Effects of preanalytical variables on the detection of proteins by immunohistochemistry in formalin-fixed, paraffin-embedded tissue. Arch Pathol Lab Med 135(5):537–543PubMedGoogle Scholar
  103. 103.
    Williams JH, Mepham BL, Wright DH (1997) Tissue preparation for immunocytochemistry. J Clin Pathol 50(5):422–428PubMedCrossRefGoogle Scholar
  104. 104.
    von Wasielewski R et al (2002) Tissue array technology for testing interlaboratory and interobserver reproducibility of immunohistochemical estrogen receptor analysis in a large multicenter trial. Am J Clin Pathol 118(5):675–682CrossRefGoogle Scholar
  105. 105.
    Atkins D et al (2004) Immunohistochemical detection of EGFR in paraffin-embedded tumor tissues: variation in staining intensity due to choice of fixative and storage time of tissue sections. J Histochem Cytochem 52(7):893–901PubMedCrossRefGoogle Scholar
  106. 106.
    Hammond ME et al (2010) American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer (unabridged version). Arch Pathol Lab Med 134(7):e48–e72PubMedGoogle Scholar
  107. 107.
    Wolff AC et al (2007) American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. Arch Pathol Lab Med 131(1):18–43PubMedGoogle Scholar
  108. 108.
    Shi SR, Liu C, Taylor CR (2007) Standardization of immunohistochemistry for formalin-fixed, paraffin-embedded tissue sections based on the antigen-retrieval technique: from experiments to hypothesis. J Histochem Cytochem 55(2):105–109PubMedCrossRefGoogle Scholar
  109. 109.
    Arber DA (2002) Effect of prolonged formalin fixation on the immunohistochemical reactivity of breast markers. Appl Immunohistochem Mol Morphol 10(2):183–186PubMedCrossRefGoogle Scholar
  110. 110.
    Pollard K et al (1987) Fixation, processing, and immunochemical reagent effects on preservation of T-lymphocyte surface membrane antigens in paraffin-embedded tissue. J Histochem Cytochem 35(11):1329–1338PubMedCrossRefGoogle Scholar
  111. 111.
    Middleton LP et al (2009) Implementation of American Society of Clinical Oncology/College of American Pathologists HER2 Guideline Recommendations in a tertiary care facility increases HER2 immunohistochemistry and fluorescence in situ hybridization concordance and decreases the number of inconclusive cases. Arch Pathol Lab Med 133(5):775–780PubMedGoogle Scholar
  112. 112.
    De Marzo AM et al (2002) Inadequate formalin fixation decreases reliability of p27 immunohistochemical staining: probing optimal fixation time using high-density tissue microarrays. Hum Pathol 33(7):756–760PubMedCrossRefGoogle Scholar
  113. 113.
    National Cancer Institute, National Institutes of Health, and U.S. Department of Health and Human Services (2007) NCI best practices for biospecimen resources. http://biospecimens.cancer.gov/global/pdfs/NCI_Best_Practices_060507.pdf. Accessed 22 June 2011
  114. 114.
    Manne U et al (1997) Re: loss of tumor marker-immunostaining intensity on stored paraffin slides of breast cancer. J Natl Cancer Inst 89(8):585–586PubMedCrossRefGoogle Scholar
  115. 115.
    Shin HJ et al (1997) Comparison of p53 immunoreactivity in fresh-cut versus stored slides with and without microwave heating. Mod Pathol 10(3):224–230PubMedGoogle Scholar
  116. 116.
    Scharl A et al (1990) Immunohistochemical detection of progesterone receptor in formalin-fixed and paraffin-embedded breast cancer tissue using a monoclonal antibody. Arch Gynecol Obstet 247(2):63–71PubMedCrossRefGoogle Scholar
  117. 117.
    Lightfoote M et al (2010) Quality assurance for design control and implementation of immunohistochemistry assays; approved Guideline, 2nd edn. Clinical and Laboratory Standards Institute (CLSI), WayneGoogle Scholar
  118. 118.
    van den Broek LJ, van de Vijver MJ (2000) Assessment of problems in diagnostic and research immunohistochemistry associated with epitope instability in stored paraffin sections. Appl Immunohistochem Mol Morphol 8(4):316–321PubMedCrossRefGoogle Scholar
  119. 119.
    Bertheau P et al (1998) Variability of immunohistochemical reactivity on stored paraffin slides. J Clin Pathol 51(5):370–374PubMedCrossRefGoogle Scholar
  120. 120.
    DiVito KA et al (2004) Long-term preservation of antigenicity on tissue microarrays. Lab Invest 84(8):1071–1078PubMedCrossRefGoogle Scholar
  121. 121.
    Jacobs TW et al (1996) Loss of tumor marker-immunostaining intensity on stored paraffin slides of breast cancer. J Natl Cancer Inst 88(15):1054–1059PubMedCrossRefGoogle Scholar
  122. 122.
    Wester K et al (2000) Paraffin section storage and immunohistochemistry. Effects of time, temperature, fixation, and retrieval protocol with emphasis on p53 protein and MIB1 antigen. Appl Immunohistochem Mol Morphol 8(1):61–70PubMedCrossRefGoogle Scholar
  123. 123.
    Fergenbaum JH et al (2004) Loss of antigenicity in stored sections of breast cancer tissue microarrays. Cancer Epidemiol Biomarkers Prev 13(4):667–672PubMedGoogle Scholar
  124. 124.
    Moslehi J et al (2010) Loss of hypoxia-inducible factor prolyl hydroxylase activity in cardiomyocytes phenocopies ischemic cardiomyopathy. Circulation 122(10):1004–1016PubMedCrossRefGoogle Scholar
  125. 125.
    Deutsch EW et al (2008) Minimum information specification for in situ hybridization and immunohistochemistry experiments (MISFISHIE). Nat Biotechnol 26(3):305–312PubMedCrossRefGoogle Scholar
  126. 126.
    Brazma A et al (2001) Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 29(4):365–371PubMedCrossRefGoogle Scholar
  127. 127.
    Masood S et al (1998) Influence of fixation, antibody clones, and signal amplification on steroid receptor analysis. Breast J 4(1):33–40CrossRefGoogle Scholar
  128. 128.
    Bromley C, Palechek P, Benda J (1994) Preservation of estrogen receptor in paraffin sections. J Histotechnol 12(2):115–118Google Scholar
  129. 129.
    Grabau D et al (1998) Influence of storage temperature and high-temperature antigen retrieval buffers on results of immunohistochemical staining in sections stored for long periods. Appl Immunohistochem 6(4):209–213CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of PathologyBrigham and Women’s Hospital, Harvard Medical SchoolBostonUSA
  2. 2.Department of Medical OncologyDana-Farber Cancer Institute, Harvard Medical SchoolBostonUSA

Personalised recommendations