Inhibition of class IA PI3K enzymes in non-small cell lung cancer cells uncovers functional compensation among isoforms

References

• Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA: Cancer J Clin 2014; 64:9-29; PMID:24399786
   PubMed Web of Science ®Google Scholar
• Stabile LP, Lyker JS, Gubish CT, Zhang W, Grandis JR, Siegfried JM. Combined targeting of the estrogen receptor and the epidermal growth factor receptor in non-small cell lung cancer shows enhanced antiproliferative effects. Cancer Res 2005; 65:1459-70; PMID:15735034; http://dx.doi.org/10.1158/0008-5472.CAN-04-1872
   PubMed Web of Science ®Google Scholar
• Pao W, Miller VA. Epidermal growth factor receptor mutations, small-molecule kinase inhibitors, and non-small-cell lung cancer: current knowledge and future directions. J Clin Oncol 2005; 23:2556-68; PMID:15767641; http://dx.doi.org/10.1200/JCO.2005.07.799
   PubMed Web of Science ®Google Scholar
• Karakas B, Bachman KE, Park BH. Mutation of the PIK3CA oncogene in human cancers. Bri J Cancer 2006; 94:455-9; PMID:16449998; http://dx.doi.org/10.1038/sj.bjc.6602970
   PubMed Web of Science ®Google Scholar
• Roberts PJ, Stinchcombe TE, Der CJ, Socinski MA. Personalized medicine in non-small-cell lung cancer: is KRAS a useful marker in selecting patients for epidermal growth factor receptor-targeted therapy? J Clin Oncol 2010; 28:4769-77; PMID:20921461; http://dx.doi.org/10.1200/JCO.2009.27.4365
   PubMed Web of Science ®Google Scholar
• Sos ML, Koker M, Weir BA, Heynck S, Rabinovsky R, Zander T, Seeger JM, Weiss J, Fischer F, Frommolt P, et al. PTEN loss contributes to erlotinib resistance in EGFR-mutant lung cancer by activation of Akt and EGFR. Cancer Res 2009; 69:3256-61; PMID:19351834; http://dx.doi.org/10.1158/0008-5472.CAN-08-4055
   PubMed Web of Science ®Google Scholar
• LoPiccolo J, Blumenthal GM, Bernstein WB, Dennis PA. Targeting the PI3K/Akt/mTOR pathway: effective combinations and clinical considerations. Drug Resist Updat 2008; 11:32-50; PMID:18166498; http://dx.doi.org/10.1016/j.drup.2007.11.003
   PubMed Web of Science ®Google Scholar
• Shaw RJ, Cantley LC. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 2006; 441:424-30; PMID:16724053; http://dx.doi.org/10.1038/nature04869
   PubMed Web of Science ®Google Scholar
• Gustafson AM, Soldi R, Anderlind C, Scholand MB, Qian J, Zhang X, Cooper K, Walker D, McWilliams A, Liu G, et al. Airway PI3K pathway activation is an early and reversible event in lung cancer development. Sci Translat Med 2010; 2:26ra5; http://dx.doi.org/10.1126/scitranslmed.3000251
   Web of Science ®Google Scholar
• Liu P, Cheng H, Roberts TM, Zhao JJ. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat Rev Drug Dis 2009; 8:627-44; PMID:19644473; http://dx.doi.org/10.1038/nrd2926
   PubMed Web of Science ®Google Scholar
• Blagden S, Olmin A, Josephs D, Stavraka C, Zivi A, Pinato DJ, Anthoney A, Decordova S, Swales K, Riisnaes R, et al. First-in-Human Study of CH5132799, an Oral Class I PI3K Inhibitor, Studying Toxicity, Pharmacokinetics, and Pharmacodynamics, in Patients with Metastatic Cancer. Clin Cancer Res 2014; 20:5908-17; PMID:25231405; http://dx.doi.org/10.1158/1078-0432.CCR-14-1315
   PubMed Web of Science ®Google Scholar
• Jia S, Roberts TM, Zhao JJ. Should individual PI3 kinase isoforms be targeted in cancer? Curr Opin Cell Biol 2009; 21:199-208; PMID:19200708; http://dx.doi.org/10.1016/j.ceb.2008.12.007
   PubMed Web of Science ®Google Scholar
• Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, Bilanges B. The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol 2010; 11:329-41; PMID:20379207; http://dx.doi.org/10.1038/nrm2882
   PubMed Web of Science ®Google Scholar
• Zhao JJ, Cheng H, Jia S, Wang L, Gjoerup OV, Mikami A, Roberts TM. The p110alpha isoform of PI3K is essential for proper growth factor signaling and oncogenic transformation. Proc Natl Acad Sci U S A 2006; 103:16296-300; PMID:17060635; http://dx.doi.org/10.1073/pnas.0607899103
   PubMed Web of Science ®Google Scholar
• Foukas LC, Claret M, Pearce W, Okkenhaug K, Meek S, Peskett E, Sancho S, Smith AJ, Withers DJ, Vanhaesebroeck B. Critical role for the p110alpha phosphoinositide-3-OH kinase in growth and metabolic regulation. Nature 2006; 441:366-70; PMID:16625210; http://dx.doi.org/10.1038/nature04694
   PubMed Web of Science ®Google Scholar
• Gupta S, Ramjaun AR, Haiko P, Wang Y, Warne PH, Nicke B, Nye E, Stamp G, Alitalo K, Downward J. Binding of ras to phosphoinositide 3-kinase p110alpha is required for ras-driven tumorigenesis in mice. Cell 2007; 129:957-68; PMID:17540175; http://dx.doi.org/10.1016/j.cell.2007.03.051
   PubMed Web of Science ®Google Scholar
• Wee S, Wiederschain D, Maira SM, Loo A, Miller C, deBeaumont R, Stegmeier F, Yao YM, Lengauer C. PTEN-deficient cancers depend on PIK3CB. Proc Natl Acad Sci U S A 2008; 105:13057-62; PMID:18755892; http://dx.doi.org/10.1073/pnas.0802655105
   PubMed Web of Science ®Google Scholar
• Jia S, Liu Z, Zhang S, Liu P, Zhang L, Lee SH, Zhang J, Signoretti S, Loda M, Roberts TM, et al. Essential roles of PI(3)K-p110beta in cell growth, metabolism and tumorigenesis. Nature 2008; 454:776-9; PMID:18594509
   PubMed Web of Science ®Google Scholar
• Guillermet-Guibert J, Bjorklof K, Salpekar A, Gonella C, Ramadani F, Bilancio A, Meek S, Smith AJ, Okkenhaug K, Vanhaesebroeck B. The p110beta isoform of phosphoinositide 3-kinase signals downstream of G protein-coupled receptors and is functionally redundant with p110gamma. Proc Natl Acad Sci U S A 2008; 105:8292-7; PMID:18544649; http://dx.doi.org/10.1073/pnas.0707761105
   PubMed Web of Science ®Google Scholar
• Puri KD, Gold MR. Selective inhibitors of phosphoinositide 3-kinase delta: modulators of B-cell function with potential for treating autoimmune inflammatory diseases and B-cell malignancies. Front Immunol 2012; 3:256; PMID:22936933; http://dx.doi.org/10.3389/fimmu.2012.00256
   PubMed Web of Science ®Google Scholar
• Herman SE, Gordon AL, Wagner AJ, Heerema NA, Zhao W, Flynn JM, Jones J, Andritsos L, Puri KD, Lannutti BJ, et al. Phosphatidylinositol 3-kinase-delta inhibitor CAL-101 shows promising preclinical activity in chronic lymphocytic leukemia by antagonizing intrinsic and extrinsic cellular survival signals. Blood 2010; 116:2078-88; PMID:20522708; http://dx.doi.org/10.1182/blood-2010-02-271171
   PubMed Web of Science ®Google Scholar
• Patrucco E, Notte A, Barberis L, Selvetella G, Maffei A, Brancaccio M, Marengo S, Russo G, Azzolino O, Rybalkin SD, et al. PI3Kgamma modulates the cardiac response to chronic pressure overload by distinct kinase-dependent and -independent effects. Cell 2004; 118:375-87; PMID:15294162; http://dx.doi.org/10.1016/j.cell.2004.07.017
   PubMed Web of Science ®Google Scholar
• Mahoney CL, Choudhury B, Davies H, Edkins S, Greenman C, Haaften G, Mironenko T, Santarius T, Stevens C, Stratton MR, et al. LKB1/KRAS mutant lung cancers constitute a genetic subset of NSCLC with increased sensitivity to MAPK and mTOR signalling inhibition. Bri J Cancer 2009; 100:370-5; PMID:19165201; http://dx.doi.org/10.1038/sj.bjc.6604886
   PubMed Web of Science ®Google Scholar
• Koivunen JP, Kim J, Lee J, Rogers AM, Park JO, Zhao X, Naoki K, Okamoto I, Nakagawa K, Yeap BY, et al. Mutations in the LKB1 tumour suppressor are frequently detected in tumours from Caucasian but not Asian lung cancer patients. Bri J Cancer 2008; 99:245-52; PMID:18594528; http://dx.doi.org/10.1038/sj.bjc.6604469
   PubMed Web of Science ®Google Scholar
• Balko JM, Potti A, Saunders C, Stromberg A, Haura EB, Black EP. Gene expression patterns that predict sensitivity to epidermal growth factor receptor tyrosine kinase inhibitors in lung cancer cell lines and human lung tumors. BMC genomics 2006; 7:289; PMID:17096850; http://dx.doi.org/10.1186/1471-2164-7-289
   PubMed Web of Science ®Google Scholar
• Jamieson S, Flanagan JU, Kolekar S, Buchanan C, Kendall JD, Lee WJ, Rewcastle GW, Denny WA, Singh R, Dickson J, et al. A drug targeting only p110alpha can block phosphoinositide 3-kinase signalling and tumour growth in certain cell types. Biochem J 2011; 438:53-62; PMID:21668414; http://dx.doi.org/10.1042/BJ20110502
   PubMed Web of Science ®Google Scholar
• Jackson SP, Schoenwaelder SM, Goncalves I, Nesbitt WS, Yap CL, Wright CE, Kenche V, Anderson KE, Dopheide SM, Yuan Y, et al. PI 3-kinase p110beta: a new target for antithrombotic therapy. Nat Med 2005; 11:507-14; PMID:15834429; http://dx.doi.org/10.1038/nm1232
   PubMed Web of Science ®Google Scholar
• Lannutti BJ, Meadows SA, Herman SE, Kashishian A, Steiner B, Johnson AJ, Byrd JC, Tyner JW, Loriaux MM, Deininger M, et al. CAL-101, a p110delta selective phosphatidylinositol-3-kinase inhibitor for the treatment of B-cell malignancies, inhibits PI3K signaling and cellular viability. Blood 2011; 117:591-4; PMID:20959606; http://dx.doi.org/10.1182/blood-2010-03-275305
   PubMed Web of Science ®Google Scholar
• Ikeda H, Hideshima T, Fulciniti M, Perrone G, Miura N, Yasui H, Okawa Y, Kiziltepe T, Santo L, Vallet S, et al. PI3K/p110{delta} is a novel therapeutic target in multiple myeloma. Blood 2010; 116:1460-8; PMID:20505158; http://dx.doi.org/10.1182/blood-2009-06-222943
   PubMed Web of Science ®Google Scholar
• Yaguchi S, Fukui Y, Koshimizu I, Yoshimi H, Matsuno T, Gouda H, Hirono S, Yamazaki K, Yamori T. Antitumor activity of ZSTK474, a new phosphatidylinositol 3-kinase inhibitor. J Natl Cancer Inst 2006; 98:545-56; PMID:16622124; http://dx.doi.org/10.1093/jnci/djj133
   PubMed Web of Science ®Google Scholar
• Weigelt B, Warne PH, Lambros MB, Reis-Filho JS, Downward J. PI3K pathway dependencies in endometrioid endometrial cancer cell lines. Clin Cancer Res 2013; 19:3533-44; PMID:23674493; http://dx.doi.org/10.1158/1078-0432.CCR-12-3815
   PubMed Web of Science ®Google Scholar
• Ihle NT, Paine-Murrieta G, Berggren MI, Baker A, Tate WR, Wipf P, Abraham RT, Kirkpatrick DL, Powis G. The phosphatidylinositol-3-kinase inhibitor PX-866 overcomes resistance to the epidermal growth factor receptor inhibitor gefitinib in A-549 human non-small cell lung cancer xenografts. Mol Cancer Ther 2005; 4:1349-57; PMID:16170026; http://dx.doi.org/10.1158/1535-7163.MCT-05-0149
   PubMed Web of Science ®Google Scholar
• Garassino MC, Martelli O, Broggini M, Farina G, Veronese S, Rulli E, Bianchi F, Bettini A, Longo F, Moscetti L, et al. Erlotinib versus docetaxel as second-line treatment of patients with advanced non-small-cell lung cancer and wild-type EGFR tumours (TAILOR): a randomised controlled trial. Lancet Oncol 2013; 14:981-8; PMID:23883922; http://dx.doi.org/10.1016/S1470-2045(13)70310-3
   PubMed Web of Science ®Google Scholar
• Kong DX, Yamori T. ZSTK474, a novel phosphatidylinositol 3-kinase inhibitor identified using the JFCR39 drug discovery system. Acta pharmacologica Sinica 2010; 31:1189-97; PMID:20729870; http://dx.doi.org/10.1038/aps.2010.150
   PubMed Web of Science ®Google Scholar
• Smith GC, Ong WK, Costa JL, Watson M, Cornish J, Grey A, Gamble GD, Dickinson M, Leung S, Rewcastle GW, et al. Extended treatment with selective phosphatidylinositol 3-kinase and mTOR inhibitors has effects on metabolism, growth, behaviour and bone strength. FEBS J 2013; 280:5337-49; PMID:23837532; http://dx.doi.org/10.1111/febs.12428
   PubMed Web of Science ®Google Scholar
• Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012; 489:519-25; PMID:22960745; http://dx.doi.org/10.1038/nature11404
   PubMed Web of Science ®Google Scholar
• Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, Herman P, Kaye FJ, Lindeman N, Boggon TJ, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004; 304:1497-500; PMID:15118125; http://dx.doi.org/10.1126/science.1099314
   PubMed Web of Science ®Google Scholar
• Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004; 350:2129-39; PMID:15118073; http://dx.doi.org/10.1056/NEJMoa040938
   PubMed Web of Science ®Google Scholar
• Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, Fujiwara S, Watanabe H, Kurashina K, Hatanaka H, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007; 448:561-6; PMID:17625570; http://dx.doi.org/10.1038/nature05945
   PubMed Web of Science ®Google Scholar
• Hammerman PS, Janne PA, Johnson BE. Resistance to Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors in Non-Small Cell Lung Cancer. Clin Cancer Res 2009; 15:7502-9; PMID:20008850; http://dx.doi.org/10.1158/1078-0432.CCR-09-0189
   PubMed Web of Science ®Google Scholar
• Courtney KD, Corcoran RB, Engelman JA. The PI3K pathway as drug target in human cancer. J Clin Oncol 2010; 28:1075-83; PMID:20085938; http://dx.doi.org/10.1200/JCO.2009.25.3641
   PubMed Web of Science ®Google Scholar
• Faber AC, Li D, Song Y, Liang MC, Yeap BY, Bronson RT, Lifshits E, Chen Z, Maira SM, Garcia-Echeverria C, et al. Differential induction of apoptosis in HER2 and EGFR addicted cancers following PI3K inhibition. Proc Natl Acad Sci U S A 2009; 106:19503-8; PMID:19850869; http://dx.doi.org/10.1073/pnas.0905056106
   PubMed Web of Science ®Google Scholar
• Engelman JA, Settleman J. Acquired resistance to tyrosine kinase inhibitors during cancer therapy. Curr Opin Genet Dev 2008; 18:73-9; PMID:18325754; http://dx.doi.org/10.1016/j.gde.2008.01.004
   PubMed Web of Science ®Google Scholar
• Yamamoto H, Shigematsu H, Nomura M, Lockwood WW, Sato M, Okumura N, Soh J, Suzuki M, Wistuba, II, Fong KM, et al. PIK3CA mutations and copy number gains in human lung cancers. Cancer Res 2008; 68:6913-21; PMID:18757405; http://dx.doi.org/10.1158/0008-5472.CAN-07-5084
   PubMed Web of Science ®Google Scholar
• Wang L, Hu H, Pan Y, Wang R, Li Y, Shen L, Yu Y, Li H, Cai D, Sun Y, et al. PIK3CA mutations frequently coexist with EGFR/KRAS mutations in non-small cell lung cancer and suggest poor prognosis in EGFR/KRAS wildtype subgroup. PloS one 2014; 9:e88291; PMID:24533074; http://dx.doi.org/10.1371/journal.pone.0088291
   PubMed Web of Science ®Google Scholar
• Maira SM, Stauffer F, Schnell C, Garcia-Echeverria C. PI3K inhibitors for cancer treatment: where do we stand? Biochem Soc Trans 2009; 37:265-72; PMID:19143644; http://dx.doi.org/10.1042/BST0370265
   PubMed Web of Science ®Google Scholar
• Hu L, Zaloudek C, Mills GB, Gray J, Jaffe RB. In vivo and in vitro ovarian carcinoma growth inhibition by a phosphatidylinositol 3-kinase inhibitor (LY294002). Clin Cancer Res 2000; 6:880-6; PMID:10741711
   PubMed Web of Science ®Google Scholar
• Edgar KA, Wallin JJ, Berry M, Lee LB, Prior WW, Sampath D, Friedman LS, Belvin M. Isoform-specific phosphoinositide 3-kinase inhibitors exert distinct effects in solid tumors. Cancer Res 2010; 70:1164-72; PMID:20103642; http://dx.doi.org/10.1158/0008-5472.CAN-09-2525
   PubMed Web of Science ®Google Scholar
• Marques M, Kumar A, Cortes I, Gonzalez-Garcia A, Hernandez C, Moreno-Ortiz MC, Carrera AC. Phosphoinositide 3-kinases p110alpha and p110beta regulate cell cycle entry, exhibiting distinct activation kinetics in G1 phase. Mol Cell Biol 2008; 28:2803-14; PMID:18285463; http://dx.doi.org/10.1128/MCB.01786-07
   PubMed Web of Science ®Google Scholar
• Marques M, Kumar A, Poveda AM, Zuluaga S, Hernandez C, Jackson S, Pasero P, Carrera AC. Specific function of phosphoinositide 3-kinase beta in the control of DNA replication. Proc Natl Acad Sci U S A 2009; 106:7525-30; PMID:19416922; http://dx.doi.org/10.1073/pnas.0812000106
   PubMed Web of Science ®Google Scholar
• Murga C, Fukuhara S, Gutkind JS. A novel role for phosphatidylinositol 3-kinase beta in signaling from G protein-coupled receptors to Akt. J Biol Chem 2000; 275:12069-73; PMID:10766839; http://dx.doi.org/10.1074/jbc.275.16.12069
   PubMed Web of Science ®Google Scholar
• Berenjeno IM, Guillermet-Guibert J, Pearce W, Gray A, Fleming S, Vanhaesebroeck B. Both p110alpha and p110beta isoforms of PI3K can modulate the impact of loss-of-function of the PTEN tumour suppressor. Biochem J 2012; 442:151-9; PMID:22150431; http://dx.doi.org/10.1042/BJ20111741
   PubMed Web of Science ®Google Scholar
• Silio V, Redondo-Munoz J, Carrera AC. Phosphoinositide 3-kinase beta regulates chromosome segregation in mitosis. Mol Biol Cell 2012; 23(23):4526-42; PMID:23051731
   PubMed Web of Science ®Google Scholar
• Utermark T, Rao T, Cheng H, Wang Q, Lee SH, Wang ZC, Iglehart JD, Roberts TM, Muller WJ, Zhao JJ. The p110alpha and p110beta isoforms of PI3K play divergent roles in mammary gland development and tumorigenesis. Gen Dev 2012; 26:1573-86; PMID:22802530; http://dx.doi.org/10.1101/gad.191973.112
   PubMed Web of Science ®Google Scholar
• Vanhaesebroeck B, Welham MJ, Kotani K, Stein R, Warne PH, Zvelebil MJ, Higashi K, Volinia S, Downward J, Waterfield MD. P110delta, a novel phosphoinositide 3-kinase in leukocytes. Proc Natl Acad Sci U S A 1997; 94:4330-5; PMID:9113989; http://dx.doi.org/10.1073/pnas.94.9.4330
   PubMed Web of Science ®Google Scholar
• Chantry D, Vojtek A, Kashishian A, Holtzman DA, Wood C, Gray PW, Cooper JA, Hoekstra MF. p110delta, a novel phosphatidylinositol 3-kinase catalytic subunit that associates with p85 and is expressed predominantly in leukocytes. J Biol Chem 1997; 272:19236-41; PMID:9235916; http://dx.doi.org/10.1074/jbc.272.31.19236
   PubMed Web of Science ®Google Scholar
• Ihle NT, Lemos R, Jr., Wipf P, Yacoub A, Mitchell C, Siwak D, Mills GB, Dent P, Kirkpatrick DL, Powis G. Mutations in the phosphatidylinositol-3-kinase pathway predict for antitumor activity of the inhibitor PX-866 whereas oncogenic Ras is a dominant predictor for resistance. Cancer Res 2009; 69:143-50; PMID:19117997; http://dx.doi.org/10.1158/0008-5472.CAN-07-6656
   PubMed Web of Science ®Google Scholar
• Herman SE, Lapalombella R, Gordon AL, Ramanunni A, Blum KA, Jones J, Zhang X, Lannutti BJ, Puri KD, Muthusamy N, et al. The role of phosphatidylinositol 3-kinase-delta in the immunomodulatory effects of lenalidomide in chronic lymphocytic leukemia. Blood 2011; 117:4323-7; PMID:21378270; http://dx.doi.org/10.1182/blood-2010-11-315705
   PubMed Web of Science ®Google Scholar
• Fruman DA, Rommel C. PI3Kdelta inhibitors in cancer: rationale and serendipity merge in the clinic. Cancer Dis 2011; 1:562-72; PMID:22586681; http://dx.doi.org/10.1158/2159-8290.CD-11-0249
   PubMed Web of Science ®Google Scholar
• Foukas LC, Berenjeno IM, Gray A, Khwaja A, Vanhaesebroeck B. Activity of any class IA PI3K isoform can sustain cell proliferation and survival. Proc Natl Acad Sci U S A 2010; 107:11381-6; PMID:20534549; http://dx.doi.org/10.1073/pnas.0906461107
   PubMed Web of Science ®Google Scholar
• Glaysher S, Bolton LM, Johnson P, Torrance C, Cree IA. Activity of EGFR, mTOR and PI3K inhibitors in an isogenic breast cell line model. BMC Res Notes 2014; 7:397; PMID:24964744; http://dx.doi.org/10.1186/1756-0500-7-397
   PubMedGoogle Scholar
• Altman SA, Randers L, Rao G. Comparison of trypan blue dye exclusion and fluorometric assays for mammalian cell viability determinations. Biotechnol Prog 1993; 9:671-4; PMID:7764357; http://dx.doi.org/10.1021/bp00024a017
   PubMed Web of Science ®Google Scholar
• O'Brien J, Wilson I, Orton T, Pognan F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem 2000; 267:5421-6; PMID:10951200; http://dx.doi.org/10.1046/j.1432-1327.2000.01606.x
   PubMedGoogle Scholar
• Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22:27-55; PMID:6382953; http://dx.doi.org/10.1016/0065-2571(84)90007-4
   PubMedGoogle Scholar