Kay Macleod

Research Summary
The deadliest aspect of the majority of human cancers is metastasis, the multi-step process by which cancer cells escape the confines of the primary site (such as breast, pancreas or other organs) and travel in the circulation to distant sites (such as brain, liver or lungs) where they can lodge, invade and grow out as secondary tumors or metastases. Many factors play into cancer metastasis including how disseminating tumor cells respond to stresses such as nutrient deprivation and altered cellular attachments. These stresses are known to activate a process known as autophagy and research in the Macleod Lab seeks to understand and clarify the role of autophagy in tumor growth and progression to metastasis. In particular, we are interested in understanding how defects in the turnover of mitochondria (the energy factory of the cell) by autophagy, leads to tumor invasion and metastasis. Using a variety of approaches from biochemical, molecular, cellular as well as genetic models to in vivo imaging and primary human patient sample analysis, research on the role of autophagy in cancer metastasis in the Macleod Lab is focused on breast cancer, pancreatic cancer and liver cancer. By examining and comparing similarities and differences between how metastasis develops from each of these organ sites, we can appreciate what new molecular targets may be most relevant to understanding and ultimately treating these deadly diseases.
Keywords
Cancer, Mitochondria, Autophagy, Stress Responses, Metastasis, Cell Migration & Invasion, Tumor metabolism
Education
  • University of Edinburgh, Scotland, B.Sc. (Hons) Molecular Biology 07/1986
  • The Beatson Institute for Cancer Research, University of Glasgow, Scotland, Ph.D. Cancer Biology 07/1990
  • Institut Pasteur, France, Post-doctoral fellow Ets Transcription Factors 03/1993
  • The Massachusetts Institute of Technology, Cambridge, MA, Post-doctoral fellow The RB tumor suppressor 09/1996
Biosciences Graduate Program Association
Publications
  1. Smith AG, Macleod KF. Autophagy, cancer stem cells and drug resistance. J Pathol. 2019 Apr; 247(5):708-718. View in: PubMed

  2. Fessenden TB, Beckham Y, Perez-Neut M, Ramirez-San Juan G, Chourasia AH, Macleod KF, Oakes PW, Gardel ML. Dia1-dependent adhesions are required by epithelial tissues to initiate invasion. J Cell Biol. 2018 04 02; 217(4):1485-1502. View in: PubMed

  3. Kathayat RS, Cao Y, Elvira PD, Sandoz PA, Zaballa ME, Springer MZ, Drake LE, Macleod KF, van der Goot FG, Dickinson BC. Active and dynamic mitochondrial S-depalmitoylation revealed by targeted fluorescent probes. Nat Commun. 2018 01 23; 9(1):334. View in: PubMed

  4. Mowers EE, Sharifi MN, Macleod KF. Functions of autophagy in the tumor microenvironment and cancer metastasis. FEBS J. 2018 05; 285(10):1751-1766. View in: PubMed

  5. Malone CF, Emerson C, Ingraham R, Barbosa W, Guerra S, Yoon H, Liu LL, Michor F, Haigis M, Macleod KF, Maertens O, Cichowski K. mTOR and HDAC Inhibitors Converge on the TXNIP/Thioredoxin Pathway to Cause Catastrophic Oxidative Stress and Regression of RAS-Driven Tumors. Cancer Discov. 2017 12; 7(12):1450-1463. View in: PubMed

  6. Qiang L, Sample A, Shea CR, Soltani K, Macleod KF, He YY. Autophagy gene ATG7 regulates ultraviolet radiation-induced inflammation and skin tumorigenesis. Autophagy. 2017; 13(12):2086-2103. View in: PubMed

  7. Drake LE, Springer MZ, Poole LP, Kim CJ, Macleod KF. Expanding perspectives on the significance of mitophagy in cancer. Semin Cancer Biol. 2017 12; 47:110-124. View in: PubMed

  8. Zhou D, Springer MZ, Xu D, Liu D, Hudmon A, Macleod KF, Meroueh SO. Small molecules inhibit STAT3 activation, autophagy, and cancer cell anchorage-independent growth. Bioorg Med Chem. 2017 06 15; 25(12):2995-3005. View in: PubMed

  9. Sharifi MN, Mowers EE, Macleod KF. Autophagic degradation of focal adhesions underlies metastatic cancer dissemination. Mol Cell Oncol. 2017; 4(2):e1198299. View in: PubMed

  10. Mowers EE, Sharifi MN, Macleod KF. Autophagy in cancer metastasis. Oncogene. 2017 03 23; 36(12):1619-1630. View in: PubMed

  11. Springer MZ, Macleod KF. In Brief: Mitophagy: mechanisms and role in human disease. J Pathol. 2016 11; 240(3):253-255. View in: PubMed

  12. Mowers EE, Sharifi MN, Macleod KF. Novel insights into how autophagy regulates tumor cell motility. Autophagy. 2016 09; 12(9):1679-80. View in: PubMed

  13. Sharifi MN, Mowers EE, Drake LE, Collier C, Chen H, Zamora M, Mui S, Macleod KF. Autophagy Promotes Focal Adhesion Disassembly and Cell Motility of Metastatic Tumor Cells through the Direct Interaction of Paxillin with LC3. Cell Rep. 2016 05 24; 15(8):1660-72. View in: PubMed

  14. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, Adhihetty PJ, Adler SG, Agam G, Agarwal R, Aghi MK, Agnello M, Agostinis P, Aguilar PV, Aguirre-Ghiso J, Airoldi EM, Ait-Si-Ali S, Akematsu T, Akporiaye ET, Al-Rubeai M, Albaiceta GM, Albanese C, Albani D, Albert ML, Aldudo J, Algül H, Alirezaei M, Alloza I, Almasan A, Almonte-Beceril M, Alnemri ES, Alonso C, Altan-Bonnet N, Altieri DC, Alvarez S, Alvarez-Erviti L, Alves S, Amadoro G, Amano A, Amantini C, Ambrosio S, Amelio I, Amer AO, Amessou M, Amon A, An Z, Anania FA, Andersen SU, Andley UP, Andreadi CK, Andrieu-Abadie N, Anel A, Ann DK, Anoopkumar-Dukie S, Antonioli M, Aoki H, Apostolova N, Aquila S, Aquilano K, Araki K, Arama E, Aranda A, Araya J, Arcaro A, Arias E, Arimoto H, Ariosa AR, Armstrong JL, Arnould T, Arsov I, Asanuma K, Askanas V, Asselin E, Atarashi R, Atherton SS, Atkin JD, Attardi LD, Auberger P, Auburger G, Aurelian L, Autelli R, Avagliano L, Avantaggiati ML, Avrahami L, Awale S, Azad N, Bachetti T, Backer JM, Bae DH, Bae JS, Bae ON, Bae SH, Baehrecke EH, Baek SH, Baghdiguian S, Bagniewska-Zadworna A, Bai H, Bai J, Bai XY, Bailly Y, Balaji KN, Balduini W, Ballabio A, Balzan R, Banerjee R, Bánhegyi G, Bao H, Barbeau B, Barrachina MD, Barreiro E, Bartel B, Bartolomé A, Bassham DC, Bassi MT, Bast RC, Basu A, Batista MT, Batoko H, Battino M, Bauckman K, Baumgarner BL, Bayer KU, Beale R, Beaulieu JF, Beck GR, Becker C, Beckham JD, Bédard PA, Bednarski PJ, Begley TJ, Behl C, Behrends C, Behrens GM, Behrns KE, Bejarano E, Belaid A, Belleudi F, Bénard G, Berchem G, Bergamaschi D, Bergami M, Berkhout B, Berliocchi L, Bernard A, Bernard M, Bernassola F, Bertolotti A, Bess AS, Besteiro S, Bettuzzi S, Bhalla S, Bhattacharyya S, Bhutia SK, Biagosch C, Bianchi MW, Biard-Piechaczyk M, Billes V, Bincoletto C, Bingol B, Bird SW, Bitoun M, Bjedov I, Blackstone C, Blanc L, Blanco GA, Blomhoff HK, Boada-Romero E, Böckler S, Boes M, Boesze-Battaglia K, Boise LH, Bolino A, Boman A, Bonaldo P, Bordi M, Bosch J, Botana LM, Botti J, Bou G, Bouché M, Bouchecareilh M, Boucher MJ, Boulton ME, Bouret SG, Boya P, Boyer-Guittaut M, Bozhkov PV, Brady N, Braga VM, Brancolini C, Braus GH, Bravo-San Pedro JM, Brennan LA, Bresnick EH, Brest P, Bridges D, Bringer MA, Brini M, Brito GC, Brodin B, Brookes PS, Brown EJ, Brown K, Broxmeyer HE, Bruhat A, Brum PC, Brumell JH, Brunetti-Pierri N, Bryson-Richardson RJ, Buch S, Buchan AM, Budak H, Bulavin DV, Bultman SJ, Bultynck G, Bumbasirevic V, Burelle Y, Burke RE, Burmeister M, Bütikofer P, Caberlotto L, Cadwell K, Cahova M, Cai D, Cai J, Cai Q, Calatayud S, Camougrand N, Campanella M, Campbell GR, Campbell M, Campello S, Candau R, Caniggia I, Cantoni L, Cao L, Caplan AB, Caraglia M, Cardinali C, Cardoso SM, Carew JS, Carleton LA, Carlin CR, Carloni S, Carlsson SR, Carmona-Gutierrez D, Carneiro LA, Carnevali O, Carra S, Carrier A, Carroll B, Casas C, Casas J, Cassinelli G, Castets P, Castro-Obregon S, Cavallini G, Ceccherini I, Cecconi F, Cederbaum AI, Ceña V, Cenci S, Cerella C, Cervia D, Cetrullo S, Chaachouay H, Chae HJ, Chagin AS, Chai CY, Chakrabarti G, Chamilos G, Chan EY, Chan MT, Chandra D, Chandra P, Chang CP, Chang RC, Chang TY, Chatham JC, Chatterjee S, Chauhan S, Che Y, Cheetham ME, Cheluvappa R, Chen CJ, Chen G, Chen GC, Chen G, Chen H, Chen JW, Chen JK, Chen M, Chen M, Chen P, Chen Q, Chen Q, Chen SD, Chen S, Chen SS, Chen W, Chen WJ, Chen WQ, Chen W, Chen X, Chen YH, Chen YG, Chen Y, Chen Y, Chen Y, Chen YJ, Chen YQ, Chen Y, Chen Z, Chen Z, Cheng A, Cheng CH, Cheng H, Cheong H, Cherry S, Chesney J, Cheung CH, Chevet E, Chi HC, Chi SG, Chiacchiera F, Chiang HL, Chiarelli R, Chiariello M, Chieppa M, Chin LS, Chiong M, Chiu GN, Cho DH, Cho SG, Cho WC, Cho YY, Cho YS, Choi AM, Choi EJ, Choi EK, Choi J, Choi ME, Choi SI, Chou TF, Chouaib S, Choubey D, Choubey V, Chow KC, Chowdhury K, Chu CT, Chuang TH, Chun T, Chung H, Chung T, Chung YL, Chwae YJ, Cianfanelli V, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016; 12(1):1-222. View in: PubMed

  15. Chourasia AH, Macleod KF. Tumor suppressor functions of BNIP3 and mitophagy. Autophagy. 2015; 11(10):1937-8. View in: PubMed

  16. Chourasia AH, Tracy K, Frankenberger C, Boland ML, Sharifi MN, Drake LE, Sachleben JR, Asara JM, Locasale JW, Karczmar GS, Macleod KF. Mitophagy defects arising from BNip3 loss promote mammary tumor progression to metastasis. EMBO Rep. 2015 Sep; 16(9):1145-63. View in: PubMed

  17. Fan X, Macleod K, Mustafi D, Conzen SD, Markiewicz E, Zamora M, Vosicky J, Mueller J, Karczmar GS. Correlation of In Vivo and Ex Vivo ADC and T2 of In Situ and Invasive Murine Mammary Cancers. PLoS One. 2015; 10(7):e0129212. View in: PubMed

  18. Chourasia AH, Boland ML, Macleod KF. Mitophagy and cancer. Cancer Metab. 2015; 3:4. View in: PubMed

  19. Sharifi MN, Mowers EE, Drake LE, Macleod KF. Measuring autophagy in stressed cells. Methods Mol Biol. 2015; 1292:129-50. View in: PubMed

  20. Fan X, Mustafi D, Markiewicz E, Zamora M, Vosicky J, Leinroth A, Mueller J, Macleod K, Conzen SD, Karczmar GS. Mammary cancer initiation and progression studied with magnetic resonance imaging. Breast Cancer Res. 2014 Dec 16; 16(6):495. View in: PubMed

  21. Markiewicz E, Fan X, Mustafi D, Zamora M, Roman BB, Jansen SA, Macleod K, Conzen SD, Karczmar GS. High resolution 3D MRI of mouse mammary glands with intra-ductal injection of contrast media. Magn Reson Imaging. 2015 Jan; 33(1):161-5. View in: PubMed

  22. Kuo WL, Sharifi MN, Lingen MW, Ahmed O, Liu J, Nagilla M, Macleod KF, Cohen EE. p62/SQSTM1 accumulation in squamous cell carcinoma of head and neck predicts sensitivity to phosphatidylinositol 3-kinase pathway inhibitors. PLoS One. 2014; 9(3):e90171. View in: PubMed

  23. Boland ML, Chourasia AH, Macleod KF. Mitochondrial dysfunction in cancer. Front Oncol. 2013 Dec 02; 3:292. View in: PubMed

  24. Drake LE, Macleod KF. Tumour suppressor gene function in carcinoma-associated fibroblasts: from tumour cells via EMT and back again? J Pathol. 2014 Feb; 232(3):283-8. View in: PubMed

  25. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, Al-Zeer MA, Albert ML, Albin RL, Alegre-Abarrategui J, Aleo MF, Alirezaei M, Almasan A, Almonte-Becerril M, Amano A, Amaravadi R, Amarnath S, Amer AO, Andrieu-Abadie N, Anantharam V, Ann DK, Anoopkumar-Dukie S, Aoki H, Apostolova N, Arancia G, Aris JP, Asanuma K, Asare NY, Ashida H, Askanas V, Askew DS, Auberger P, Baba M, Backues SK, Baehrecke EH, Bahr BA, Bai XY, Bailly Y, Baiocchi R, Baldini G, Balduini W, Ballabio A, Bamber BA, Bampton ET, Bánhegyi G, Bartholomew CR, Bassham DC, Bast RC, Batoko H, Bay BH, Beau I, Béchet DM, Begley TJ, Behl C, Behrends C, Bekri S, Bellaire B, Bendall LJ, Benetti L, Berliocchi L, Bernardi H, Bernassola F, Besteiro S, Bhatia-Kissova I, Bi X, Biard-Piechaczyk M, Blum JS, Boise LH, Bonaldo P, Boone DL, Bornhauser BC, Bortoluci KR, Bossis I, Bost F, Bourquin JP, Boya P, Boyer-Guittaut M, Bozhkov PV, Brady NR, Brancolini C, Brech A, Brenman JE, Brennand A, Bresnick EH, Brest P, Bridges D, Bristol ML, Brookes PS, Brown EJ, Brumell JH, Brunetti-Pierri N, Brunk UT, Bulman DE, Bultman SJ, Bultynck G, Burbulla LF, Bursch W, Butchar JP, Buzgariu W, Bydlowski SP, Cadwell K, Cahová M, Cai D, Cai J, Cai Q, Calabretta B, Calvo-Garrido J, Camougrand N, Campanella M, Campos-Salinas J, Candi E, Cao L, Caplan AB, Carding SR, Cardoso SM, Carew JS, Carlin CR, Carmignac V, Carneiro LA, Carra S, Caruso RA, Casari G, Casas C, Castino R, Cebollero E, Cecconi F, Celli J, Chaachouay H, Chae HJ, Chai CY, Chan DC, Chan EY, Chang RC, Che CM, Chen CC, Chen GC, Chen GQ, Chen M, Chen Q, Chen SS, Chen W, Chen X, Chen X, Chen X, Chen YG, Chen Y, Chen Y, Chen YJ, Chen Z, Cheng A, Cheng CH, Cheng Y, Cheong H, Cheong JH, Cherry S, Chess-Williams R, Cheung ZH, Chevet E, Chiang HL, Chiarelli R, Chiba T, Chin LS, Chiou SH, Chisari FV, Cho CH, Cho DH, Choi AM, Choi D, Choi KS, Choi ME, Chouaib S, Choubey D, Choubey V, Chu CT, Chuang TH, Chueh SH, Chun T, Chwae YJ, Chye ML, Ciarcia R, Ciriolo MR, Clague MJ, Clark RS, Clarke PG, Clarke R, Codogno P, Coller HA, Colombo MI, Comincini S, Condello M, Condorelli F, Cookson MR, Coombs GH, Coppens I, Corbalan R, Cossart P, Costelli P, Costes S, Coto-Montes A, Couve E, Coxon FP, Cregg JM, Crespo JL, Cronjé MJ, Cuervo AM, Cullen JJ, Czaja MJ, D'Amelio M, Darfeuille-Michaud A, Davids LM, Davies FE, De Felici M, de Groot JF, de Haan CA, De Martino L, De Milito A, De Tata V, Debnath J, Degterev A, Dehay B, Delbridge LM, Demarchi F, Deng YZ, Dengjel J, Dent P, Denton D, Deretic V, Desai SD, Devenish RJ, Di Gioacchino M, Di Paolo G, Di Pietro C, Díaz-Araya G, Díaz-Laviada I, Diaz-Meco MT, Diaz-Nido J, Dikic I, Dinesh-Kumar SP, Ding WX, Distelhorst CW, Diwan A, Djavaheri-Mergny M, Dokudovskaya S, Dong Z, Dorsey FC, Dosenko V, Dowling JJ, Doxsey S, Dreux M, Drew ME, Duan Q, Duchosal MA, Duff K, Dugail I, Durbeej M, Duszenko M, Edelstein CL, Edinger AL, Egea G, Eichinger L, Eissa NT, Ekmekcioglu S, El-Deiry WS, Elazar Z, Elgendy M, Ellerby LM, Eng KE, Engelbrecht AM, Engelender S, Erenpreisa J, Escalante R, Esclatine A, Eskelinen EL, Espert L, Espina V, Fan H, Fan J, Fan QW, Fan Z, Fang S, Fang Y, Fanto M, Fanzani A, Farkas T, Farré JC, Faure M, Fechheimer M, Feng CG, Feng J, Feng Q, Feng Y, Fésüs L, Feuer R, Figueiredo-Pereira ME, Fimia GM, Fingar DC, Finkbeiner S, Finkel T, Finley KD, Fiorito F, Fisher EA, Fisher PB, Flajolet M, Florez-McClure ML, Florio S, Fon EA, Fornai F, Fortunato F, Fotedar R, Fowler DH, Fox HS, Franco R, Frankel LB, Fransen M, Fuentes JM, Fueyo J, Fujii J, Fujisaki K, Fujita E, Fukuda M, Furukawa RH, Gaestel M, Gailly P, Gajewska M, Galliot B, Galy V, Ganesh S, Ganetzky B, Ganley IG, Gao FB, Gao GF, Gao J, Garcia L, Garcia-Manero G, Garcia-Marcos M, Garmyn M, Gartel AL, Gatti E, Gautel M, Gawriluk TR, Gegg ME, Geng J, Germain M, Gestwicki JE, Gewirtz DA, Ghavami S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012 Apr; 8(4):445-544. View in: PubMed

  26. Glick D, Zhang W, Beaton M, Marsboom G, Gruber M, Simon MC, Hart J, Dorn GW, Brady MJ, Macleod KF. BNip3 regulates mitochondrial function and lipid metabolism in the liver. Mol Cell Biol. 2012 Jul; 32(13):2570-84. View in: PubMed

  27. De Raedt T, Walton Z, Yecies JL, Li D, Chen Y, Malone CF, Maertens O, Jeong SM, Bronson RT, Lebleu V, Kalluri R, Normant E, Haigis MC, Manning BD, Wong KK, Macleod KF, Cichowski K. Exploiting cancer cell vulnerabilities to develop a combination therapy for ras-driven tumors. Cancer Cell. 2011 Sep 13; 20(3):400-13. View in: PubMed

  28. Szmulewitz RZ, Clark R, Lotan T, Otto K, Taylor Veneris J, Macleod K, Rinker-Schaeffer C. MKK4 suppresses metastatic colonization by multiple highly metastatic prostate cancer cell lines through a transient impairment in cell cycle progression. Int J Cancer. 2012 Feb 01; 130(3):509-20. View in: PubMed

  29. Macleod KF. The RB tumor suppressor: a gatekeeper to hormone independence in prostate cancer? J Clin Invest. 2010 Dec; 120(12):4179-82. View in: PubMed

  30. Barth S, Glick D, Macleod KF. Autophagy: assays and artifacts. J Pathol. 2010 Jun; 221(2):117-24. View in: PubMed

  31. Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010 May; 221(1):3-12. View in: PubMed

  32. Liu H, Knabb JR, Spike BT, Macleod KF. Elevated poly-(ADP-ribose)-polymerase activity sensitizes retinoblastoma-deficient cells to DNA damage-induced necrosis. Mol Cancer Res. 2009 Jul; 7(7):1099-109. View in: PubMed

  33. Macleod KF. The role of the RB tumour suppressor pathway in oxidative stress responses in the haematopoietic system. Nat Rev Cancer. 2008 Oct; 8(10):769-81. View in: PubMed

  34. Taylor JL, Szmulewitz RZ, Lotan T, Hickson J, Griend DV, Yamada SD, Macleod K, Rinker-Schaeffer CW. New paradigms for the function of JNKK1/MKK4 in controlling growth of disseminated cancer cells. Cancer Lett. 2008 Dec 08; 272(1):12-22. View in: PubMed

  35. Lotan T, Hickson J, Souris J, Huo D, Taylor J, Li T, Otto K, Yamada SD, Macleod K, Rinker-Schaeffer CW. c-Jun NH2-terminal kinase activating kinase 1/mitogen-activated protein kinase kinase 4-mediated inhibition of SKOV3ip.1 ovarian cancer metastasis involves growth arrest and p21 up-regulation. Cancer Res. 2008 Apr 01; 68(7):2166-75. View in: PubMed

  36. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, Biard-Piechaczyk M, Blum JS, Bredesen DE, Brodsky JL, Brumell JH, Brunk UT, Bursch W, Camougrand N, Cebollero E, Cecconi F, Chen Y, Chin LS, Choi A, Chu CT, Chung J, Clarke PG, Clark RS, Clarke SG, Clavé C, Cleveland JL, Codogno P, Colombo MI, Coto-Montes A, Cregg JM, Cuervo AM, Debnath J, Demarchi F, Dennis PB, Dennis PA, Deretic V, Devenish RJ, Di Sano F, Dice JF, Difiglia M, Dinesh-Kumar S, Distelhorst CW, Djavaheri-Mergny M, Dorsey FC, Dröge W, Dron M, Dunn WA, Duszenko M, Eissa NT, Elazar Z, Esclatine A, Eskelinen EL, Fésüs L, Finley KD, Fuentes JM, Fueyo J, Fujisaki K, Galliot B, Gao FB, Gewirtz DA, Gibson SB, Gohla A, Goldberg AL, Gonzalez R, González-Estévez C, Gorski S, Gottlieb RA, Häussinger D, He YW, Heidenreich K, Hill JA, Høyer-Hansen M, Hu X, Huang WP, Iwasaki A, Jäättelä M, Jackson WT, Jiang X, Jin S, Johansen T, Jung JU, Kadowaki M, Kang C, Kelekar A, Kessel DH, Kiel JA, Kim HP, Kimchi A, Kinsella TJ, Kiselyov K, Kitamoto K, Knecht E, Komatsu M, Kominami E, Kondo S, Kovács AL, Kroemer G, Kuan CY, Kumar R, Kundu M, Landry J, Laporte M, Le W, Lei HY, Lenardo MJ, Levine B, Lieberman A, Lim KL, Lin FC, Liou W, Liu LF, Lopez-Berestein G, López-Otín C, Lu B, Macleod KF, Malorni W, Martinet W, Matsuoka K, Mautner J, Meijer AJ, Meléndez A, Michels P, Miotto G, Mistiaen WP, Mizushima N, Mograbi B, Monastyrska I, Moore MN, Moreira PI, Moriyasu Y, Motyl T, Münz C, Murphy LO, Naqvi NI, Neufeld TP, Nishino I, Nixon RA, Noda T, Nürnberg B, Ogawa M, Oleinick NL, Olsen LJ, Ozpolat B, Paglin S, Palmer GE, Papassideri I, Parkes M, Perlmutter DH, Perry G, Piacentini M, Pinkas-Kramarski R, Prescott M, Proikas-Cezanne T, Raben N, Rami A, Reggiori F, Rohrer B, Rubinsztein DC, Ryan KM, Sadoshima J, Sakagami H, Sakai Y, Sandri M, Sasakawa C, Sass M, Schneider C, Seglen PO, Seleverstov O, Settleman J, Shacka JJ, Shapiro IM, Sibirny A, Silva-Zacarin EC, Simon HU, Simone C, Simonsen A, Smith MA, Spanel-Borowski K, Srinivas V, Steeves M, Stenmark H, Stromhaug PE, Subauste CS, Sugimoto S, Sulzer D, Suzuki T, Swanson MS, Tabas I, Takeshita F, Talbot NJ, Tallóczy Z, Tanaka K, Tanaka K, Tanida I, Taylor GS, Taylor JP, Terman A, Tettamanti G, Thompson CB, Thumm M, Tolkovsky AM, Tooze SA, Truant R, Tumanovska LV, Uchiyama Y, Ueno T, Uzcátegui NL, van der Klei I, Vaquero EC, Vellai T, Vogel MW, Wang HG, Webster P, Wiley JW, Xi Z, Xiao G, Yahalom J, Yang JM, Yap G, Yin XM, Yoshimori T, Yu L, Yue Z, Yuzaki M, Zabirnyk O, Zheng X, Zhu X, Deter RL. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008 Feb; 4(2):151-75. View in: PubMed

  37. Dirlam A, Spike BT, Macleod KF. Deregulated E2f-2 underlies cell cycle and maturation defects in retinoblastoma null erythroblasts. Mol Cell Biol. 2007 Dec; 27(24):8713-28. View in: PubMed

  38. Spike BT, Macleod KF. Effects of hypoxia on heterotypic macrophage interactions. Cell Cycle. 2007 Nov 01; 6(21):2620-4. View in: PubMed

  39. Tracy K, Macleod KF. Regulation of mitochondrial integrity, autophagy and cell survival by BNIP3. Autophagy. 2007 Nov-Dec; 3(6):616-9. View in: PubMed

  40. Tracy K, Dibling BC, Spike BT, Knabb JR, Schumacker P, Macleod KF. BNIP3 is an RB/E2F target gene required for hypoxia-induced autophagy. Mol Cell Biol. 2007 Sep; 27(17):6229-42. View in: PubMed

  41. Spike BT, Dibling BC, Macleod KF. Hypoxic stress underlies defects in erythroblast islands in the Rb-null mouse. Blood. 2007 Sep 15; 110(6):2173-81. View in: PubMed

  42. Diwan A, Koesters AG, Odley AM, Pushkaran S, Baines CP, Spike BT, Daria D, Jegga AG, Geiger H, Aronow BJ, Molkentin JD, Macleod KF, Kalfa TA, Dorn GW. Unrestrained erythroblast development in Nix-/- mice reveals a mechanism for apoptotic modulation of erythropoiesis. Proc Natl Acad Sci U S A. 2007 Apr 17; 104(16):6794-9. View in: PubMed

  43. Liu HP, Thompson AM, Macleod KF. A novel form of pRb expressed during normal myelopoiesis and in tumour-associated macrophages. Cell Prolif. 2005 Feb; 38(1):13-24. View in: PubMed

  44. Spike BT, Macleod KF. The Rb tumor suppressor in stress responses and hematopoietic homeostasis. Cell Cycle. 2005 Jan; 4(1):42-5. View in: PubMed

  45. Spike BT, Dirlam A, Dibling BC, Marvin J, Williams BO, Jacks T, Macleod KF. The Rb tumor suppressor is required for stress erythropoiesis. EMBO J. 2004 Oct 27; 23(21):4319-29. View in: PubMed

  46. Liu H, Dibling B, Spike B, Dirlam A, Macleod K. New roles for the RB tumor suppressor protein. Curr Opin Genet Dev. 2004 Feb; 14(1):55-64. View in: PubMed

  47. Lipinski MM, Macleod KF, Williams BO, Mullaney TL, Crowley D, Jacks T. Cell-autonomous and non-cell-autonomous functions of the Rb tumor suppressor in developing central nervous system. EMBO J. 2001 Jul 02; 20(13):3402-13. View in: PubMed

  48. Macleod KF, Jacks T. Insights into cancer from transgenic mouse models. J Pathol. 1999 Jan; 187(1):43-60. View in: PubMed

  49. Tsai KY, Hu Y, Macleod KF, Crowley D, Yamasaki L, Jacks T. Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol Cell. 1998 Sep; 2(3):293-304. View in: PubMed

  50. Macleod KF, Hu Y, Jacks T. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J. 1996 Nov 15; 15(22):6178-88. View in: PubMed

  51. Plaza S, Grevin D, MacLeod K, Stehelin D, Saule S. Pax-QNR/Pax-6, a paired- and homeobox-containing protein, recognizes Ets binding sites and can alter the transactivating properties of Ets transcription factors. Gene Expr. 1994; 4(1-2):43-52. View in: PubMed

  52. Macleod KF, Sherry N, Hannon G, Beach D, Tokino T, Kinzler K, Vogelstein B, Jacks T. p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 1995 Apr 15; 9(8):935-44. View in: PubMed

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  55. Plumb M, Frampton J, Wainwright H, Walker M, Macleod K, Goodwin G, Harrison P. GATAAG; a cis-control region binding an erythroid-specific nuclear factor with a role in globin and non-globin gene expression. Nucleic Acids Res. 1989 Jan 11; 17(1):73-92. View in: PubMed

  56. Isamat M, Macleod KF, King A, McEwan C, Melton DW. Characterization, evolutionary relationships, and chromosome location of processed mouse HPRT pseudogene. Somat Cell Mol Genet. 1988 Jul; 14(4):359-69. View in: PubMed

  57. Harrison PR, Plumb M, Frampton J, Thiele B, Macleod K, Chester J, Chambers I, Fleming J, O'Prey J, Walker M, et al. Regulation of erythroid-specific gene expression. Biomed Biochim Acta. 1990; 49(2-3):S5-10. View in: PubMed

  58. Macleod K, Plumb M. Derepression of mouse beta-major-globin gene transcription during erythroid differentiation. Mol Cell Biol. 1991 Sep; 11(9):4324-32. View in: PubMed

  59. Macleod K, Leprince D, Stehelin D. The ets gene family. Trends Biochem Sci. 1992 Jul; 17(7):251-6. View in: PubMed