- Email: [email protected]
My journey with Bruce Sidell
Comparative Biochemistry and Physiology, Part D 6 (2011) 337–338
Contents lists available at ScienceDirect
Comparative Biochemistry and Physiology, Part D j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c b p d
Obituary
My journey with Bruce Sidell Bruce Sidell was born on March 20, 1948. I joined the world 9 weeks later setting off parallel lives that bridged to yield personal richness and professional interactions during a geographic and intellectual journey. I take this opportunity to share parts of this passage with you, in part for personal gratification but also in part to present an example of the importance of engaging compatible colleagues. We both received our first degrees in 1970. Bruce went on to do his M.Sc. (1972) and Ph.D. (1975) with Ladd Prosser at the University of Illinois. I did my M.Sc. (1972) at the University of Toronto with Betty Roots who had just finished a period in the Prosser laboratory and my Ph.D. (1975) with Peter Hochachka who was an intellectual disciple of Prosser. We both did two year postdocs, Bruce at John Hopkins University and I at Pennsylvania State University, and thereafter assumed Assistant Professorships. Bruce took up his post at the University of Maine in Orono, while I was situated 320 miles due north at Mount Allison University in Sackville, New Brunswick, Canada. At the time we were the only two vertebrate comparative physiologists/biochemists on the north eastern seaboard. We both proceeded through the academic ranks and paid our dues as senior administrators, Bruce as Director of the School of Marine Sciences, and I as a V.P. (Academic and Research). With mutual support our sanities prevailed and we returned to the professoriate for the last chapter of our careers. I first met Bruce shortly after our arrivals on the east coast, a meeting that led to a long friendship. We both had children with overlapping ages, so our families became great friends as well. We summered together at the Mount Desert Island Biological Laboratory (MDIBL) and arranged a sabbatical year together in 1983–84 in Ian Johnston's laboratory in St. Andrews, Scotland. Bruce and I worked at the bench together in a number of places including: the MDIBL; St. Andrews, Scotland; the Marine Laboratory, Plymouth, England; Manus, Brazil with Drs. Vera and Adalberto Val; and of course Palmer Station, Antarctica where Bruce spent many field seasons. Our specific collaborative efforts were directed mostly toward metabolic fuel preference in heart and skeletal muscle involving studies with fish, representatives of all of the other vertebrate classes, and unexpectedly cephalopods (e.g. 1–5). In the broad sense we actually did not coauthor many papers together. Our agreement was that a necessity for co-authorship was that we both must have had hands on involvement. In hindsight, what is much more interesting to me is how ideas and projects moved seamlessly over the years from one laboratory to another. I present below two examples of our wonderful synergy. Bruce was interested in the impact of acute temperature change and temperature acclimation on energy metabolism from the date of his first publication with Prosser (6) to his final work in this area with George Somero (7). During the 1980s, Bruce's group published a series of papers that set models for experimental design and conceptual advancement in linking field and laboratory studies (e.g., doi:10.1016/j.cbd.2011.06.006
8,9). I did not become directly interested in this area of inquiry until about 1990 when we embarked on a series of studies related to temperature, fuel preference, and heart performance (e.g. 10). Our collective work led us to conclude that low temperature resulted in an enhanced utilization of lipids as metabolic fuels, at least in heart and skeletal muscle and led to detailed studies at specific loci. Here we focussed on the enzymes carnitine palmitoyltransferase (11,12) and fatty acid acyl CoA synthetase (13,14). A most interesting aspect of this area was the fatty acid binding protein (FABP). My laboratory first reported the presence of FABP in teleost fish by exploiting hearts that lack myoglobin. Both myoglobin and FABP have similar molecular weights, so in effect nature did the first step in purification for us (15). At the same time Bruce and Jeff Hazel had designed an elegant chamber for measuring diffusion of small molecules in aqueous solutions (16) and we were able to use this apparatus to show that FABP actually did function to accelerate the movement of fatty acids (17). At this point further intellectual inquiry exceeded my skills but Bruce's team went on to reveal aspects such as increased levels of FABP at low temperature (e.g. (18)) and multiple isoforms of the protein (19). In 1981, we reported that numerous species of common North Atlantic fishes had white hearts once the blood was flushed out. We attributed the color to the lack of myoglobin. Bruce was an intellectual party to this finding as evidenced by a short note we co-authored in the MDIBL Bulletin (20); however, true to our practice, his name did not appear on the publication in the primary literature (21). Many years later though he did prove beyond reasonable doubt that the hearts of these fish lacked myoglobin (22). Much work though was conducted between these publications. My group provided the first empirical evidence that myoglobin supported oxygen consumption in working hearts (e.g. 23–25). Bruce confirmed this fundamental finding in Antarctic icefish (26) and then took this program to places that were not on my radar. By exploiting species of hemoglobin-less Antarctic fish but with variable levels of heart myoglobin he executed studies at the level of molecular biology to explain the genetic lesions leading to the loss of myoglobin protein (27,28). From this emerged some of Bruce's last great thinking of the connection among myoglobin, nitric oxide levels, and angiogenesis that could actually lead to the evolutionary success of icefish (29,30). I could go on with other examples in areas such as anerobic metabolism, contractile performance, and sarcoplasmic reticulum but I think the point has been made. Bruce and I started our careers as independent scientists at institutions that at the time did not place a high priority on research. We were geographically isolated from the mainstream of science and formed a two person support group. I cannot speak for Bruce on this point but I know it was great fortune for me. His early death is a pity as we were preparing to pack our pipettes once again in pursuit of interesting animals around the world. In one of our last conversations
338
W.R. Driedzic / Comparative Biochemistry and Physiology, Part D 6 (2011) 337–338
he declared that he was “going on the next trip himself”. I miss him dearly. References [1] Sidell, B.D., Driedzic, W.R., Stowe, D.B., Johnston, I.A., 1987]. Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol. Zool. 60, 221–232. [2] Driedzic, W.R., Sidell, B.D., Stowe, D.B., Branscombe, R., 1987]. Matching of vertebrate cardiac energy demand to energy metabolism: enzyme activity levels and high-energy phosphates. Am. J. Physiol. 252, R930–R937. [3] Driedzic, W.R., Sidell, B.D., Stewart, J.M., Johnston, I.A., 1990]. Maximal activities of enzymes of energy metabolism in cephalopod systemic and branchial hearts. Physiol. Zool. 63, 615–629. [4] Sidell, B.D., Crockett, E.L., Driedzic, W.R., 1995]. Antarctic fish tissues preferentially catabolize monoenoic fatty acids. J. Exp. Zool. 271, 73–81. [5] West, J.L., Bailey, J.R., Almeida-Val, V.M.F., Val, A.L., Sidell, B.D., Driedzic, W.R., 1999]. Activity levels of enzymes of energy metabolism in heart and red muscle are higher in north-temperate-zone than in Amazonian teleosts. Can. J. Zool. 77, 690–696. [6] Sidell, B.D., Wilson, F.R., Hazel, J.R., Prosser, C.L., 1973]. Time course of thermal acclimation in goldfish. J. Comp. Physiol. 84, 119–127. [7] Kawall, H.G., Torres, J.J., Sidell, B.D., Somero, G.N., 2002]. Metabolic cold adaptation in Antarctic fishes: evidence from enzymatic activities of brain. Mar. Biol. 140, 279–286. [8] Stone, B.B., Sidell, B.D., 1981]. Metabolic responses of striped bass (Morone saxatilis) to temperature acclimation. I. Alterations in carbon sources for hepatic energy metabolism. J. Exp. Zool. 218, 371–379. [9] Kleckner, N.W., Sidell, B.D., 1985]. Comparison of maximal activities of enzymes from tissues of thermally-acclimated and naturally-acclimatized chain pickerel, (Esox niger). Physiol. Zool. 58, 18–28. [10] Bailey, J.R., Driedzic, W.R., 1993]. Influence of low temperature acclimation on fate of metabolic fuels in rainbow trout (Onchorhynchus mykiss) hearts. Can. J. Zool. 71, 2167–2173. [11] Rodnick, K.J., Sidell, B.D., 1994]. Cold-acclimation increases carnitine palmitoyltransferase I activity in oxidative muscle of striped bass. Am. J. Physiol. 266, R405–R412. [12] Patey, C.P., Driedzic, W.R., 1997]. Cold acclimation increases activities of mitochondrial long-chain acyl-CoA synthetase and carnitine acyl-CoA transferase I in heart of rainbow trout (Oncorhynchus mykiss). Can. J. Zool. 75, 324–331. [13] Hicks, J.M.T., Bailey, J.R., Driedzic, W.R., 1996]. Acclimation to low temperature is associated with an increase in long-chain acyl-CoA synthetase in rainbow trout (Oncorynchus mykiss) heart. Can. J. Zool. 74, 1–7 Erratum: Can J Zool 74, 1786. [14] Grove, T.J., Sidell, B.D., 2004]. Fatty acyl CoA synthetase from Antarctic notothenioid fishes may influence substrate specificity of fat oxidation. Comp. Biochem. Physiol. B 139, 53–63. [15] Stewart, J.M., Driedzic, W.R., 1988]. Fatty acid binding proteins in teleost fish. Can. J. Zool. 66, 2671–2675. [16] Hazel, J.R., Sidell, B.D., 1987]. A new method for determining diffusion coefficients for small molecules in aqueous solution. Anal. Biochem. 166, 335–341.
[17] Stewart, J.M., Berkelaar, J.A.M., Driedzic, W.R., 1991]. Fatty acid binding protein facilitates the diffusion of oleate in a model system. Biochem. J. 275, 569–573. [18] Londraville, R.L., Sidell, B.D., 1996]. Cold acclimation increases fatty acid-binding protein concentration in aerobic muscle of striped bass, Morone saxatilis. J. Exp. Zool. 275, 36–44. [19] Vayda, M.E., Londraville, R.L., Cashon, R., Costello, L., Sidell, B.D., 1998]. Two distinct types of fatty acid-binding protein are expressed in heart ventricle of Antarctic fishes. Biochem. J. 330, 375–382. [20] Driedzic, W.R., Sidell, B.D., Stewart, J.M., 1981]. Myoglobin content and maximal activities of enzymes of energy metabolism in fish white heart and skeletal muscle. Bull. Mt. Desert Is. Biol. Lab. 20, 32–34. [21] Driedzic, W.R., Stewart, J.M., 1982]. Myoglobin content and the activities of the enzymes of energy metabolism in red and white fish hearts. J. Comp. Physiol. 149, 67–73. [22] Grove, T.J., Sidell, B.D., 2002]. Myoglobin deficiency in the hearts of phylogenetically diverse Temperate Zone fish species. Can. J. Zool. 80, 833–901. [23] Driedzic, W.R., Stewart, J.M., Scott, D.L., 1982]. The protective effect of myoglobin during hypoxic perfusion of isolated fish hearts. J. Mol. Cell. Cardiol. 14, 673–677. [24] Bailey, J.R., Driedzic, W.R., 1986]. Function of myoglobin in oxygen consumption by isolated perfused fish hearts. Am. J. Physiol. 251, R1144–R1150. [25] Bailey, J.R., Sephton, D.H., Driedzic, W.R., 1990]. Oxygen uptake by isolated perfused fish hearts with differing myoglobin concentrations under hypoxic conditions. J. Mol. Cell. Cardiol. 22, 1125–1134. [26] Acierno, R., Agnisola, C., Tota, B., Sidell, B.D., 1997]. Myoglobin enhances cardiac performance in Antarctic icefish species that express the protein. Am. J. Physiol. 273, R100–R106. [27] Small, D.J., Moylan, T.J., Vayda, M.E., Sidell, B.D., 2003]. The myoglobin gene of the Antarctic icefish (Chaenocephalus aceratus) contains a duplicated TATAAAA sequence that interferes with transcription. J. Exp. Biol. 206, 131–139. [28] Grove, T.J., Hendrickson, J., Sidell, B.D., 2004]. Two species of Antarctic icefishes (genus Champsocephalus) share a common genetic lesion leading to the loss of myoglobin expression. Polar Biol. 27, 579–585. [29] Garafaolo, F., Amelio, D., Cerra, M.C., Tota, B., Sidell, B.D., Pelligrino, D., 2009]. Morphological and physiological study of the cardiac NOS–NO system in the Antarctic (Hb−/Mb−) icefish, Chaenocephalus aceratus and the red-blooded Trematomus bernacchii. Nitric Oxide 20, 69–78. [30] Beers, J.M., Borley, K.A., Sidell, B.D., 2010]. Relationship among circulating hemoglobin, nitric oxide synthase activities and angiogenic poise in red- and white-blooded Antarctic notothenioid fishes. Comp. Biochem. Physiol. A 156, 422–429.
William R. Driedzic Ocean Sciences Centre, Memorial University of Newfoundland St. John's, N.L., Canada, A1C 5S7 Tel.: + 1 709 864 3282; fax: +1 709 864 3220. E-mail address: [email protected].
Contents lists available at ScienceDirect
Comparative Biochemistry and Physiology, Part D j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c b p d
Obituary
My journey with Bruce Sidell Bruce Sidell was born on March 20, 1948. I joined the world 9 weeks later setting off parallel lives that bridged to yield personal richness and professional interactions during a geographic and intellectual journey. I take this opportunity to share parts of this passage with you, in part for personal gratification but also in part to present an example of the importance of engaging compatible colleagues. We both received our first degrees in 1970. Bruce went on to do his M.Sc. (1972) and Ph.D. (1975) with Ladd Prosser at the University of Illinois. I did my M.Sc. (1972) at the University of Toronto with Betty Roots who had just finished a period in the Prosser laboratory and my Ph.D. (1975) with Peter Hochachka who was an intellectual disciple of Prosser. We both did two year postdocs, Bruce at John Hopkins University and I at Pennsylvania State University, and thereafter assumed Assistant Professorships. Bruce took up his post at the University of Maine in Orono, while I was situated 320 miles due north at Mount Allison University in Sackville, New Brunswick, Canada. At the time we were the only two vertebrate comparative physiologists/biochemists on the north eastern seaboard. We both proceeded through the academic ranks and paid our dues as senior administrators, Bruce as Director of the School of Marine Sciences, and I as a V.P. (Academic and Research). With mutual support our sanities prevailed and we returned to the professoriate for the last chapter of our careers. I first met Bruce shortly after our arrivals on the east coast, a meeting that led to a long friendship. We both had children with overlapping ages, so our families became great friends as well. We summered together at the Mount Desert Island Biological Laboratory (MDIBL) and arranged a sabbatical year together in 1983–84 in Ian Johnston's laboratory in St. Andrews, Scotland. Bruce and I worked at the bench together in a number of places including: the MDIBL; St. Andrews, Scotland; the Marine Laboratory, Plymouth, England; Manus, Brazil with Drs. Vera and Adalberto Val; and of course Palmer Station, Antarctica where Bruce spent many field seasons. Our specific collaborative efforts were directed mostly toward metabolic fuel preference in heart and skeletal muscle involving studies with fish, representatives of all of the other vertebrate classes, and unexpectedly cephalopods (e.g. 1–5). In the broad sense we actually did not coauthor many papers together. Our agreement was that a necessity for co-authorship was that we both must have had hands on involvement. In hindsight, what is much more interesting to me is how ideas and projects moved seamlessly over the years from one laboratory to another. I present below two examples of our wonderful synergy. Bruce was interested in the impact of acute temperature change and temperature acclimation on energy metabolism from the date of his first publication with Prosser (6) to his final work in this area with George Somero (7). During the 1980s, Bruce's group published a series of papers that set models for experimental design and conceptual advancement in linking field and laboratory studies (e.g., doi:10.1016/j.cbd.2011.06.006
8,9). I did not become directly interested in this area of inquiry until about 1990 when we embarked on a series of studies related to temperature, fuel preference, and heart performance (e.g. 10). Our collective work led us to conclude that low temperature resulted in an enhanced utilization of lipids as metabolic fuels, at least in heart and skeletal muscle and led to detailed studies at specific loci. Here we focussed on the enzymes carnitine palmitoyltransferase (11,12) and fatty acid acyl CoA synthetase (13,14). A most interesting aspect of this area was the fatty acid binding protein (FABP). My laboratory first reported the presence of FABP in teleost fish by exploiting hearts that lack myoglobin. Both myoglobin and FABP have similar molecular weights, so in effect nature did the first step in purification for us (15). At the same time Bruce and Jeff Hazel had designed an elegant chamber for measuring diffusion of small molecules in aqueous solutions (16) and we were able to use this apparatus to show that FABP actually did function to accelerate the movement of fatty acids (17). At this point further intellectual inquiry exceeded my skills but Bruce's team went on to reveal aspects such as increased levels of FABP at low temperature (e.g. (18)) and multiple isoforms of the protein (19). In 1981, we reported that numerous species of common North Atlantic fishes had white hearts once the blood was flushed out. We attributed the color to the lack of myoglobin. Bruce was an intellectual party to this finding as evidenced by a short note we co-authored in the MDIBL Bulletin (20); however, true to our practice, his name did not appear on the publication in the primary literature (21). Many years later though he did prove beyond reasonable doubt that the hearts of these fish lacked myoglobin (22). Much work though was conducted between these publications. My group provided the first empirical evidence that myoglobin supported oxygen consumption in working hearts (e.g. 23–25). Bruce confirmed this fundamental finding in Antarctic icefish (26) and then took this program to places that were not on my radar. By exploiting species of hemoglobin-less Antarctic fish but with variable levels of heart myoglobin he executed studies at the level of molecular biology to explain the genetic lesions leading to the loss of myoglobin protein (27,28). From this emerged some of Bruce's last great thinking of the connection among myoglobin, nitric oxide levels, and angiogenesis that could actually lead to the evolutionary success of icefish (29,30). I could go on with other examples in areas such as anerobic metabolism, contractile performance, and sarcoplasmic reticulum but I think the point has been made. Bruce and I started our careers as independent scientists at institutions that at the time did not place a high priority on research. We were geographically isolated from the mainstream of science and formed a two person support group. I cannot speak for Bruce on this point but I know it was great fortune for me. His early death is a pity as we were preparing to pack our pipettes once again in pursuit of interesting animals around the world. In one of our last conversations
338
W.R. Driedzic / Comparative Biochemistry and Physiology, Part D 6 (2011) 337–338
he declared that he was “going on the next trip himself”. I miss him dearly. References [1] Sidell, B.D., Driedzic, W.R., Stowe, D.B., Johnston, I.A., 1987]. Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol. Zool. 60, 221–232. [2] Driedzic, W.R., Sidell, B.D., Stowe, D.B., Branscombe, R., 1987]. Matching of vertebrate cardiac energy demand to energy metabolism: enzyme activity levels and high-energy phosphates. Am. J. Physiol. 252, R930–R937. [3] Driedzic, W.R., Sidell, B.D., Stewart, J.M., Johnston, I.A., 1990]. Maximal activities of enzymes of energy metabolism in cephalopod systemic and branchial hearts. Physiol. Zool. 63, 615–629. [4] Sidell, B.D., Crockett, E.L., Driedzic, W.R., 1995]. Antarctic fish tissues preferentially catabolize monoenoic fatty acids. J. Exp. Zool. 271, 73–81. [5] West, J.L., Bailey, J.R., Almeida-Val, V.M.F., Val, A.L., Sidell, B.D., Driedzic, W.R., 1999]. Activity levels of enzymes of energy metabolism in heart and red muscle are higher in north-temperate-zone than in Amazonian teleosts. Can. J. Zool. 77, 690–696. [6] Sidell, B.D., Wilson, F.R., Hazel, J.R., Prosser, C.L., 1973]. Time course of thermal acclimation in goldfish. J. Comp. Physiol. 84, 119–127. [7] Kawall, H.G., Torres, J.J., Sidell, B.D., Somero, G.N., 2002]. Metabolic cold adaptation in Antarctic fishes: evidence from enzymatic activities of brain. Mar. Biol. 140, 279–286. [8] Stone, B.B., Sidell, B.D., 1981]. Metabolic responses of striped bass (Morone saxatilis) to temperature acclimation. I. Alterations in carbon sources for hepatic energy metabolism. J. Exp. Zool. 218, 371–379. [9] Kleckner, N.W., Sidell, B.D., 1985]. Comparison of maximal activities of enzymes from tissues of thermally-acclimated and naturally-acclimatized chain pickerel, (Esox niger). Physiol. Zool. 58, 18–28. [10] Bailey, J.R., Driedzic, W.R., 1993]. Influence of low temperature acclimation on fate of metabolic fuels in rainbow trout (Onchorhynchus mykiss) hearts. Can. J. Zool. 71, 2167–2173. [11] Rodnick, K.J., Sidell, B.D., 1994]. Cold-acclimation increases carnitine palmitoyltransferase I activity in oxidative muscle of striped bass. Am. J. Physiol. 266, R405–R412. [12] Patey, C.P., Driedzic, W.R., 1997]. Cold acclimation increases activities of mitochondrial long-chain acyl-CoA synthetase and carnitine acyl-CoA transferase I in heart of rainbow trout (Oncorhynchus mykiss). Can. J. Zool. 75, 324–331. [13] Hicks, J.M.T., Bailey, J.R., Driedzic, W.R., 1996]. Acclimation to low temperature is associated with an increase in long-chain acyl-CoA synthetase in rainbow trout (Oncorynchus mykiss) heart. Can. J. Zool. 74, 1–7 Erratum: Can J Zool 74, 1786. [14] Grove, T.J., Sidell, B.D., 2004]. Fatty acyl CoA synthetase from Antarctic notothenioid fishes may influence substrate specificity of fat oxidation. Comp. Biochem. Physiol. B 139, 53–63. [15] Stewart, J.M., Driedzic, W.R., 1988]. Fatty acid binding proteins in teleost fish. Can. J. Zool. 66, 2671–2675. [16] Hazel, J.R., Sidell, B.D., 1987]. A new method for determining diffusion coefficients for small molecules in aqueous solution. Anal. Biochem. 166, 335–341.
[17] Stewart, J.M., Berkelaar, J.A.M., Driedzic, W.R., 1991]. Fatty acid binding protein facilitates the diffusion of oleate in a model system. Biochem. J. 275, 569–573. [18] Londraville, R.L., Sidell, B.D., 1996]. Cold acclimation increases fatty acid-binding protein concentration in aerobic muscle of striped bass, Morone saxatilis. J. Exp. Zool. 275, 36–44. [19] Vayda, M.E., Londraville, R.L., Cashon, R., Costello, L., Sidell, B.D., 1998]. Two distinct types of fatty acid-binding protein are expressed in heart ventricle of Antarctic fishes. Biochem. J. 330, 375–382. [20] Driedzic, W.R., Sidell, B.D., Stewart, J.M., 1981]. Myoglobin content and maximal activities of enzymes of energy metabolism in fish white heart and skeletal muscle. Bull. Mt. Desert Is. Biol. Lab. 20, 32–34. [21] Driedzic, W.R., Stewart, J.M., 1982]. Myoglobin content and the activities of the enzymes of energy metabolism in red and white fish hearts. J. Comp. Physiol. 149, 67–73. [22] Grove, T.J., Sidell, B.D., 2002]. Myoglobin deficiency in the hearts of phylogenetically diverse Temperate Zone fish species. Can. J. Zool. 80, 833–901. [23] Driedzic, W.R., Stewart, J.M., Scott, D.L., 1982]. The protective effect of myoglobin during hypoxic perfusion of isolated fish hearts. J. Mol. Cell. Cardiol. 14, 673–677. [24] Bailey, J.R., Driedzic, W.R., 1986]. Function of myoglobin in oxygen consumption by isolated perfused fish hearts. Am. J. Physiol. 251, R1144–R1150. [25] Bailey, J.R., Sephton, D.H., Driedzic, W.R., 1990]. Oxygen uptake by isolated perfused fish hearts with differing myoglobin concentrations under hypoxic conditions. J. Mol. Cell. Cardiol. 22, 1125–1134. [26] Acierno, R., Agnisola, C., Tota, B., Sidell, B.D., 1997]. Myoglobin enhances cardiac performance in Antarctic icefish species that express the protein. Am. J. Physiol. 273, R100–R106. [27] Small, D.J., Moylan, T.J., Vayda, M.E., Sidell, B.D., 2003]. The myoglobin gene of the Antarctic icefish (Chaenocephalus aceratus) contains a duplicated TATAAAA sequence that interferes with transcription. J. Exp. Biol. 206, 131–139. [28] Grove, T.J., Hendrickson, J., Sidell, B.D., 2004]. Two species of Antarctic icefishes (genus Champsocephalus) share a common genetic lesion leading to the loss of myoglobin expression. Polar Biol. 27, 579–585. [29] Garafaolo, F., Amelio, D., Cerra, M.C., Tota, B., Sidell, B.D., Pelligrino, D., 2009]. Morphological and physiological study of the cardiac NOS–NO system in the Antarctic (Hb−/Mb−) icefish, Chaenocephalus aceratus and the red-blooded Trematomus bernacchii. Nitric Oxide 20, 69–78. [30] Beers, J.M., Borley, K.A., Sidell, B.D., 2010]. Relationship among circulating hemoglobin, nitric oxide synthase activities and angiogenic poise in red- and white-blooded Antarctic notothenioid fishes. Comp. Biochem. Physiol. A 156, 422–429.
William R. Driedzic Ocean Sciences Centre, Memorial University of Newfoundland St. John's, N.L., Canada, A1C 5S7 Tel.: + 1 709 864 3282; fax: +1 709 864 3220. E-mail address: [email protected].