OXYGEN SENSING MOLECULE TO MAN
OXYGEN SENSINGMOLECULE TO MAN
ADVANCES IN EXPERIMENTAL MEDICINE AND BIOLOGY
Editorial Board:NATHAN BACK, State University of New York at BuffaloIRUN R. COHEN, The Weizmann Institute of ScienceDAVID KRITCHEVSKY, Wistar InstituteABEL LAJTHA, N. S. Kline Institute for Psychiatric ResearchRODOLFO PAOLETTI, University of Milan
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OXYGEN SENSINGMOLECULE TO MAN
Edited by
Sukhamay LahiriUniversity of Pennsylvania Medical CenterPhiladelphia, Pennsylvania
Nanduri R. PrabhakarCase Western Reserve UniversityCleveland, Ohio
and
Robert E. Forster, IIUniversity of Pennsylvania Medical CenterPhiladelphia, Pennsylvania
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PREFACE
By a close vote in Chile, 1996, the membership decided to hold the XIVmeeting of the International Society of Arterial Chemoreception (ISAC) inPhiladelphia,, USA, with Sukhamay Lahiri as its president.
The XIV meeting of the ISAC was held on June 24-28, 1999, in Philadelphia.Since its inception, these meetings have been focused on arterial chemoreceptors andtheir functions. This time, it was expanded to include oxygen sensing in other tissuesand cells in the body, and the genes involved. This genetic flavour made the meetingmore exciting, and it was attended by more than two hundred participants at a time.The idea was to bring together scientists from cellular and systemic boundaries ofphysiology, working at the interface of cellular and molecular biology. As a result, anew conference was born and the title of the conference was Oxygen Sensing: Moleculeto Man. The organizers of the conference were Sukhamay Lahiri and NanduriPrabhakar,
Dr. Robert W. Torrance died on January 8, 1999. C.C. Michel who was astudent of his and was close to him presented a Tribute. Two other students of his,Mark Hanson and Prem Kumar, also wrote reminiscences. Bob also collaborated withPatricio Zapata in Chile occasionally during the last few years. Patricio and Carolinaalso wrote a reminiscence. Bob was a founder member of the ISAC, and as thepresident of the Oxford meeting, 1966, when he wrote a seminal article, prolegomena,reviewing the state of knowledge of arterial chemoreception at that time. This articlewas a landmark in the history of chemoreception.
One special feature of the symposium was that twelve experts had been askedto write articles for a volume of Respiration Physiology pertaining to the symposium,which was precirculated to the participants. This volume gave a preview of thesymposium, thanks to the Editor of Respiration Physiology, Dr. Peter Scheid. It wasto provide a focus for the participants and background reading for the forthcomingmeeting.
The first two days of the symposium were devoted to the genes and geneticexpression of oxygen sensing, beginning with systemic phenomena in man andanimals. It quickly went onto bacteria and yeast, bringing out how similar their oxygensensing was to the mammals at the molecular level. As the meeting proceeded, itbecame clear that oxygen sensing in mammals can be divided primarily into twodistinct categories: one is the membrane based NAD(P)H oxidase systems and anotheris mitochondrial. These were present in various cells and systems. A controversyarose as to how more oxygen radicals are generated during hypoxia. It was felt that thedifferences probably pertained to demanding methods using fluorescent dye. Potassiumion channels figured most prominently in the glomus cell membrane depolarization.Inhibition of the classical oxygen sensitive potassium currents did not inhibit oxygensensing, as a result the role of voltage insensitive leak potassium current was
v
resurrected, in addition to the of voltage sensitive HERG–like potassium current in allthe glomus cells. Several features of glomus cells fit the criteria of oxygenchemoreceptors but their sensory discharge did not always fit these criteria. It wastherefore proposed that sensory nerves may be the ultimate sensors whereas glomuscells play only a secretory role, but recoding from the petrosal ganglion cells did notsupport this notion.
There were fourteen papers from the young investigators competing for theawards, four of whom were judged winners by the audience: two for the Heymans-deCastro-Neil Awards, (Beth Ann Summers and Roger J. Thompson) and two forComroe, Forster & Lambertsen Awards (Ricardo Pardal and Nicholas A. Ritucci).
There was a roundtable conference at the end of the second day, discussingthe genomic aspects. A similar roundtable conference was originally planned to takeplace at the end of fourth day but by then there had been so much discussion that it wasfelt unnecessary.
The original gramophone recordings of the carotid body sensory discharged,which were made in the 1930s by Drs. Zotterman, von Euler,and Liljestrand, wereplayed to the audience at the banquet. We are grateful to Professor Curt von Euler,Karolinska Institut, Stockholm, Sweden, for the gift.
The council of the ISAC met and at a business meeting the membershipdecided on the venue of the next meeting which is to be Lyon, France, in 2002, withJean-Marc Pequignot as its president. Tentatively the meeting after that is to be heldin Kita-kyushu, Japan,in 2005. There will be a section on Arterial Chemoreception atIUPS Meeting in New Zealand,in 2001.
The Symposium was only possible because of the funds made available to usby generous gifts, particularly from the Barra Foundation, US Army ResearchAdministration, Ecosystems Tech Transfer, Inc.,and by Merck & Company, and for thecontribution of David E. Millhorn. The Division of Lung Diseases National Heart,Lung,and Blood Institute provided a conference grant (R13-III–60955). We are alsofortunate to have received additional anonymous donations. We are grateful to themall.
Finally, we are grateful to the participants who came and contributed to thesuccess of the Symposium. Special thanks are due to Mrs. Mary Pili (University ofPennsylvania, Philadelphia, PA., USA) and Mrs. Marianne Sperk (Case WesternReserve University, Cleveland, Ohio, USA) and Mrs. Michele Deparc, Ruhr-Universityat Bochum, Germany, for their secretarial managements.
The EditorsSukhamay Lahiri (Philadelphia, PA, USA)Nanduri R. Prabhakar (Cleveland, OH, USA)Robert E. Forster, II (Philadelphia, PA, USA)
August 12, 1999
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CONTENTS
A Tribute to Robert W. Torrance................................................ 1Charles C. Michel
Reminiscence of Bob Torrance (1) ............................................. 7Patricio and Carolina Zapata
Reminiscence of Bob Torrance (2) ........................................... 9Mark Hanson and Prem Kumar
Genomics of Oxygen Sensing
Placticity and Multiplicity in the Mechanisms of Oxygen Sensing ....... 13Sukhamay Lahiri
Evolution of Human Hypoxia Tolerance Physiology ........................ 25Peter W. Hochachka, and C. Carlos Monge
Comparative Aspects of High-Altitude Adaptation in HumanPopulations.......................................................................................... 45
Lorna G. Moore, V. Fernando Armaza, Mercedes Villena,and Enrique Vargas
Tibetan and Andean Contrasts in Adaptation to High-AltitudeHypoxia............................................................................................ 63
Cynthia M. Beall
A Genomic Model for Differential Hypoxic Ventilatory Responses .... 75Clarke G. Tankersley
Regulation of the Hypoxia-Inducible : ARNT is notnecessary for hypoxic induction of in the nucleus .................. 87
Max Gassman, Dmitri Chilov, and Roland H. Wenger
Intracellular Pathways Linking Hypoxia to Activation of c-fos andAP-1.................................................................................. 101Daniel R. Premkumar, Gautam Adhikary, Jeffery L. Overholt,Michael S. Simonson, Neil S. Cherniack, andNanduri R. Prabhakar
vii
Hypoxia-Induced Regulation of mRNA Stability ...................................... 111Waltke R. Paulding and Maria Czyzyk-Krzeska
Hypoxia, HIF-1, and the Pathophysiology of Common Human Diseases..... 123Gregg L. Semenza, Faton Agani, David Feldser, Narayan Iyer,Lori Kotch, Erik Laughner, and Aimee Yu
Gene Regulation during Hypoxia in Excitable Oxygen-Sensing Cells:Depolarization-Transcription Coupling ............................................................. 131
David E. Millhorn, Dana Beitner-Johnson, Laura Conforti,P. William Conrad, Suichi Kobayashi, Yong Yuan, and Randy Rust
Regulation of CREB by Moderate Hypoxia in PC 12 Cells............................ 143Dana Beitner-Johnson, Randy T. Rust, Tyken Hsieh, and DavidE. Millhorn
Reactive Oxygen Species as Regulators of Oxygen Dependent GeneExpression................................................................................................. 153
Jochim Fandrey and Just Genius
A Glycolytic Pathway to Apoptosis of Hypoxic Cardiac Myocytes:Molecular Pathways of Increased Acid Production .................................. 161
Keith A. Webster, Daryl J. Discher, Olga M. Hernandez,Kazuhito Yamashita, and Nanette H. Bishorpric
Mitochondrial-Nuclear Crosstalk Is Involved in Oxygen-Regulated GeneExpression in Yeast................................................................................ 177
Robert O. Poyton and Christopher J. Dagsgaard
Rox1 Mediated Repression: Oxygen dependent repression in yeast............ 185Alexander J. Kastaniotis, and Richard S. Zitomer
Oxygen Dependence of Expression of Cytochrome c and Cytochrome cOxidase Genes in S. cerevisiae ................................................................... 197
Pastricia V. Burke, and Kurt E. Kwast
Hypoxic and Redox Inhibition of the Human Cardiac L-TypeChannel........................................................................................... 209
I.M. Fearon, A.C.V. Palmer, A.J. Balmforth, S.G. Ball,G. Varadi, and C. Peers
Molecular Identification of and Poassium Channels inthe Pulmonary Circulation ........................................................................ 219
Stephen L. Archer, E. Kenneth Weir, Helen L. Reeve, andEvangelos Michelakis
viii
Chemosensing at the Carotid Body: Involvement of a HERG-likepotassium current in glomus cells ...................................................... 241
Jeffrey L. Overholt, Eckhard Ficker, Tianen Yang, HashimShams, Gary R. Bright, and Nanduri R. Prabhakar
Oxidant Signalling and Vascular Oxygen Sensing: Role of inResponses of the Bovine Pulmonary Artery to Changes in ............... 249
Kamal M. Mohazzab-H. and Michael C. Wolin
Tissue and Mitochondrial Enzymes: Cytochrome c Oxidase as asSensor.............................................................................................. 259
D.F. Wilson, A. Mokashi, S. Lahiri, and S.A. Vinogradov
Regulation of Shaker-Type Potassium Channels by Hypoxia:Oxygen-sensitive channels in PC12 cells ...................................... 265
Laura Conforti and David E. Millhorn
HIF-1 Is Essential for Multilineage Hematopoiesis in the Embryo ......... 275David M. Adelman, Emin Maltepe, and M. Celeste Simon
Dual Influence of Nitric Oxide on Gene Regulation during Hypoxia ...... 285Gautam Adhikary, Daniel R.D. Premkumar, andNanduri R. Prabhakar
Hypoxia Differentially Regulates the Mitogen- and Stress-ActivatedProtein Kinases: Role of in the activation ofMAPK and p38y .............................................................................. 293
P. William Conrad, David E. Millhorn, and Dana Beitner-Johnson
Chairman’s Summary: Mechanisms of Oxygen Homeostasis,Circa 1999 ......................................................................................... 303
Gregg L. Semenza
Arterial Chemoreceptors
Oxygen, Homeostasis, and Metabolic Regulation ................................... 311Peter W. Hochachka
Evidence that Nitric Oxide Plays a Role in Sensing from TissueNO and Measurements in Cat Carotid Body .................................. 337
Donald G. Buerk and Sukhamay Lahiri
Carotid Body Gap Junctions: Secretion of Transmitters and PossibleElectric Coupling between Glomus Cells and Nerve Terminals .............. 349
Carlos Eyzaguirre
ix
Short- and Long-Term Regulation of Rat Carotid Body Gap Junctions bycAMP Identification of Connexin43, a Gap Junction Subunit............... 359
Verónica Abudara, Carloa Eyzaguirre, and Juan C. Sáez
Subcellular Localization and Function of B-Type Cytochromes inCarotid Body and Other Paraganglionic Cells ..................................... 371
Wolfgang Kummer, Brigette Höhler, Anna Goldenberg,andBettina Lange
Acetylcholine Sensitivity of Cat Petrosal Ganglion Neurons ................. 377Machiko Shirahata, Yumiko Ishizawa, Maria Rudisill,James S.K. Sham, Brian Schofield, and Robert S. Fitzgerald
Responses of Petrosal Ganglion Neurons in vitro to Hypoxic Stimuliand Putative Transmitters ............................................................... 389
J. Alcayaga, R. Varas, J. Arroyo, R. Iturriaga, and P. Zapata
The Metabolic Hypothesis Revisited .................................................. 397Charmaine Rozanov, Arijit Roy, Anil Mokashi,Shinobu Osanai, Peter Daudu, Bayard Storey, andSukhamay Lahiri
Effect of Adenosine on Chemosenstivity, Functional, Cellularand Molecular Studies ........................................................................ 405
P. Kumar, A.F. Conway, C. Vandier, N.J. Marshall,J. Bruynseels, and G.M. Matthews
The Present Status of the Mechanical Hypothesis for ChemoreceptorStimulation............................................................................................ 411
Ashima Anand and A.S. Paintal
Identification of An Oxygen-Sensitive Potassium Channel in NeonatalRat Carotid Body Type I Cells .......................................................... 419
Betrice A. Williams and Keith J. Buckler
Significancy of ROS in Oxygen Chemoreception in the Carotid BodyChemoreception: Apparent Lack of a Role of NADPH Oxidase .... . . . . . . . 425
A. Obeso, G. Sanz-Flfayate, M.T. Agapito , and C. Gonzalez
ATP-Dependent and Voltage-Gated Channels in EndothelialCells of Brain Capillaries: Effect of Hypoxia ..................................... 435
Marco A. Delpiano
Different Mechanisms by Different Channels................ 441Gabriel C. Haddad and Huajun Liu
x
Response of Intracellular pH to Acute Anoxia in Individual Neuronsfrom Chemosensitive and Nonchemosensitive Regions of the Medulla..... 453
Laura Chambers-Kersh, Nick A. Ritucci, Jay B. Dean, andRobert W. Putnam
Hyperbaric Oxygen Depolarized Solitary Complex Neurons inTissue Slices of Rat Medulla Oblongata ............................................. 465
Daniel K. Mulkey, Richard A. Henderson III, and Jay B. Dean
Chronic Hypoxia Induces Changes in the Central Nervous SystemProcessing of Arterial Chemoreceptor Input......................................... 477
M.R. Dwinell, K.A. Huey, and F.L. Powell
Acetylcholine Is Released from in vitro Cat Carotid Bodies duringHypoxic Stimulation.............................................................................. 485
R.S. Fitzgerald, M. Shirahata, and H-Y. Wang
Interactions between Acetylcholine and Dopamine in Chemoreception..... 495P. Zapata, C. Larraín, R. Iturriaga, J. Alcayaga, and C. Eyzauirre
Interactions between Catecholamines and Neuropeptides in the CarotidBody: Evidence for Dopamine Modulation of Neutral EndopeptidaseActivity..................................................................................................... 507
Ganesh K. Kumar, Eui K. Oh, and Myeong-Seon Lee
Pharmacological Effecs of Endothelin in Rat Carotid Body: Activation ofSecond Messenger Pathways and Potentiation of ChemoreceptorActivity.................................................................................................... 517
J. Chen, L. He, B. Dinger, and S. Fidone
Oxygen and Acid Chemoreception by Pheochromocytoma (PC 12) Cells.... 527S.C. Taylor and C. Peers
Postnatal Changes in Cardiovascular Regulation during Hypoxia .............. 539Phyllis M. Gootman and Norman Gootman
Expression and Localization of A2a and Al-Adenosine Receptor Genesin the Rat Carotid Body and Petrosala Ganglia: A2a and A1-adenosinereceptor mRNAs in the rat carotid body ................................................. 549
E.B. Gauda
Serotonin and the Hypoxic Ventilatory Response in Awake Goats .......... 559J.K. Herman, K.D. O’Halloran, and G.E. Bisgard
xi
Peripheral Chemosensitivity in Mutant Mice Deficient in Nitric OxideSynthase.................................................................................................. 571
David D. Kline and Nanduri R. Prabhakar
Dopaminergix Excitation in Goat Carotid Body May be Mediated bySerotonin Receptors ...... ........................................................................ 581
K.D. O’Halloran, J.K. Herman, P.L. Janssen, and G.E. Bisgard
Augmentation of Calcium Current by Hypoxia in Carotid BodyGlomus Cells........................................................................................ 589
B.A. Summers, J.L. Overholt, and N.R. Prabhakar
in Developing Rat Adrenal Chromaffin Cells ......... 601Roger J. Thompson and Colin A. Nurse
by Model Airway Chemoreceptors: Hypoxic inhibition ofchannels in H146 cells .................................................................... 611
Ita O’Kelly, Chris Peers, and Paul J. Kemp
Morphological Adaptation of the Peptidergic Innervation to ChronicHypoxia in the Rat Carotid Body ........................................................ 623
H. Matsuda, T. Kusakabe, Y. Hayashida, F.L. Powell,M.H. Ellisman, T. Kawakami, and T. Takenaka
Continuous But Not Episodic Hypoxia Induces CREB Phosphorylationin Rat Carotid Body Type I Cells .......................................................... 631
Z.-Y. Wang, T.L. Baker, I.M. Keith, G.S. Mitchell, andG.E. Bisgard
Intracellular of the Carotid Body .................................................... 637D.F. Wilson, S.M. Evans, C. Rozanov, A. Roy, C.J. Koch,K.M. Laughlin, and S. Lahiri
Redox-Based Inhibition of Channel/Current Is Not Related to HypoxicChemosensory Responses in Rat Carotid Body ........................................ 645
Arijit Roy, Charmaine Rozanov, Anil Mokashi, andSukhamay Lahiri
Effects of 2, 4-Dinitrophenol (DNP) on the Relationship betweenIntracellular Calcium of Glomus Cells and Chemosensory Activitiesof the Rat Carotid Body ........................................................................... 655
Peter A. Dauda, Charmaine Rosanov, Arijit Roy, Anil Mokashi,and Sukhamay Lahiri
xii
Estimation of Chemosensitivity from the Carotid Body in Humans .... 663M. Tanaka, A. Masuda, T. Kobayashi, and Y. Honda
Adenosine-Dopamine Interactions and Ventilation Mediated throughCarotid Body Chemoreceptors .............................................................. 671
Emilia C. Monteiro and J. Alexandre Ribeiro
Carotid Body NO-CO Interaction and Chronic Hypoxia .......................... 685C. Di Giulio, A. Grillo, I. Ciocca, M.A. Macrì, F. Daniele,G. Sabatino, M. Cacchio, M.A. De Lutiis, R. Da Porto,F. Di Natale, and M. Felaco
Interplay between the Cytosolic Increase and Potential Changes inGlomus Cells in Response to Chemical Stimuli..................................... 691
Yoshiaki Hayashida, Katsuaki Yoshizaki, and Tatsumi Kusakabe
Characteristics of Carotid Body Chemosensitivity in the Mouse: BaselineStudies for Future Experiments with Knockout Animals ........................ 697
L. He, J. Chen, B. Dinger, and S. Fidone
Role of Substance P in Neutral Endopeptidase Modulation of HypoxicResponse of the Carotid Body ............................................................ 705
Ganesh K. Kumar, Yu Ru-Kou, Jeffrey F. Overholt, andNanduri R. Prabhakar
Effect of Barium on Rat Carotid Body Glomus Cell and CarotidChemosensory Response........................................................................ 715
A. Mokashi, A. Roy, C. Rozanov, P. Daudu, and S. Lahiri
A Dual-Acid Influx Transport System in the Carotid Body Type ICell: Acid influx in carotid body type I cells .......................................... 723
Ke-Li Tsai, Richard D. Vaughan-Jones, and Keith J. Buckler
L-Dopa and High Oxygen Influence Release of Catecholamines fromthe Cat Carotid Body ........................................................................... 733
Hay-Yan J. Wang, Machiko Shirahata, and Robert S. Fitzgerald
Effects of a Dopamine Agonist on Cytosolic Changes Induced byHypoxia in Rat Glomus Cells ................................................................ 743
Katsuaki Yoshizaki, Hideki Momiyama, and Yoshiaki Hayashida
Carotid Chemoreceptors Participation in Brain Glucose Regulation:Role of arginine-vasopressin .................................................................. 749
Sergio A. Montero, Alexander Yarkov, and Ramon Alvarez-Buylla
xiii
Nitric Oxide Modulation of Carotid Chemoreception ............................ 761Rodrigo Iturriaga, Sandra Villanueva, and Julio Alcayaga
and Respiration in Exercising Human Muscle: The Regulation ofOxidative Phosphorylation in vivo .............................................................. 769
Youngran Chung, Paul Mole, Tuan K. Tran, Ulrike Kreutzer,Napapon Sailasuta, Ralph Hurd, and Thomas Jue
pH Sensitivity in the Isolated CNS of Newborn Mouse ............................. 785Claudia D. Infante and Jaime Eugenin
Aortic Body Chemoreflex of the Anesthetized Rat: Electrophysiologicalmorphological and reflex studies ........................................................... 789
James F.X. Jones
Changes in the Peptidergic Innervation of the Rat Carotid Body a Monthafter the Termination of Chonic Hypoxia ................................................ 793
T. Kusakabe, Y. Hayashida, H. Matsuda, T. Kawakami, andT. Takenaka
Carotid Bodies and the Sigh Reflex in the Conscious and AnesthetisedGuine-Pig.................................................................................................... 801
Daryl O. Schwenke and Patricia A. Cragg
Immunohistochemical Study of the Carotid Body during Hibernation....... 815Kazuo Ohtomo, Kohko Fukurara, and Katsuaki Yoshizaki
Neurochemical Reorganization of Chemoreflex Pathway after CarotidBody Denervation in Rats....................................................................... 823
J.C. Roux, J. Peyronnet, O. Pascual, Y. Dalmaz, andJ.M. Pequignot
Index.......................................................................................................... 829
xiv