Frontiers in Protein and Peptide Sciences

Volume: 1

Oxygen Binding Properties and Tetrameric Stability of Hemoglobins From the Snakes Crotalus Durissus Terrificus and Liophis Miliaris

Author(s): Fábio Renato Lombardi, Maristella Conte Anazetti, Giovanni César Santos, Patrícia Peres Polizelli, Johnny Rizzieri Olivieri, Walter Filgueira de Azevedo and Gustavo Orlando Bonilla-Rodriguez

Pp: 3-30 (28)

DOI: 10.2174/9781608058624114010004

* (Excluding Mailing and Handling)

Abstract

Hemoglobins (Hbs) from the South American snake Liophis miliaris undergo a reversible oxygen-linked dissociation phenomenon α2β2 + 4O2 ↔ 2αβ(O2), due to substituted glutamate residues (43β and 101β) at the α1β2- interface, according to Matsuura et al., 1989. This work reports the oxygen-binding properties and analysis of tetrameric stability from the major hemoglobins of two snakes: a terrestrial species (Crotalus durissus terrificus), and a semiaquatic one, L. miliaris. The major hemoglobins from both species were analyzed by classic functional experimental approaches and other analytical techniques: dimer-tetramer association constant by analytical gel filtration chromatography and small angle x-ray scattering (SAXS). In addition, we performed molecular modeling of the hemoglobin from L. miliaris. The functional results display cooperative oxygen binding, alkaline Bohr Effect, and conformational transitions, a behavior which is compatible with tetrameric Hbs. Also, the estimated dimer-tetramer association constant 4K2, radius of gyration, and maximum dimension exhibit similar compatibility. A molecular modeling of the structure of L. miliaris Hb, on the other hand, allows us to conclude that the residues Glu43β(CD2) and Glu101β(G3) are not essential in the maintenance of the tetrameric form, supporting our findings and allowing us to rule out the hypothesis proposed in the literature for the Hb of Liophis miliaris and other species of snakes. Therefore, the results reported in the paper suggest that the major Hbs of Liophis miliaris and Crotalus durissus terrificus are stable tetramers in vivo and in vitro.


Keywords: Crotalus durissus terrificus, Dimer-tetramer association constant, Hemoglobin, Liophis miliaris, Oxygen binding properties and SAXS.

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      • 16. vendor/laravel/framework/src/Illuminate/Routing/ControllerDispatcher.php:43
      • 17. vendor/laravel/framework/src/Illuminate/Routing/Route.php:260
    • (select j.user_access_id,j.volume_id,j.user_id,j.from_ip,j.to_ip,j.type,j.track,"Trial Access" as access_base_text, CASE j.type WHEN 111 THEN true ELSE false END as terms_popup, "S" as content_download_type, null as restricted_user_access_key, null as restricted_user_access_type, CASE j.track WHEN 0 THEN false ELSE true END as tracksAccessByVolume,"chapter" as access_level, j.chapter_id from `user_access_chapter_trail` as `j` inner join `user_access_info` as `info` on `j`.`user_access_id` = `info`.`user_access_id` where ((j.from_ip <= 309824417 and j.to_ip >=309824417 )) and ((j.from_date <= 1740347465 and j.to_date >= 1740347465 and j.perpetual= 0) or (j.from_date is null and j.to_date is null and j.perpetual= 1)) and j.chapter_id = 6545) union (select j.user_access_id,j.volume_id,j.user_id,j.from_ip,j.to_ip,j.type,j.track,"Subscribed" as access_base_text, false as terms_popup, "S" as content_download_type, null as restricted_user_access_key, null as restricted_user_access_type, CASE j.track WHEN 0 THEN false ELSE true END as tracksAccessByVolume,"chapter" as access_level, j.chapter_id from `user_access_chapter_corporate` as `j` inner join `user_access_info` as `info` on `j`.`user_access_id` = `info`.`user_access_id` where ((j.from_ip <= 309824417 and j.to_ip >=309824417 )) and ((j.from_date <= 1740347465 and j.to_date >= 1740347465 and j.perpetual= 0) or (j.from_date is null and j.to_date is null and j.perpetual= 1)) and j.chapter_id = 6545) union (select j.user_access_id,j.volume_id,j.user_id,j.from_ip,j.to_ip,j.type,j.track,"Token Based Access" as access_base_text, false as terms_popup, "R" as content_download_type, j.uc_id as restricted_user_access_key, "v" as restricted_user_access_type, CASE j.track WHEN 0 THEN false ELSE true END as tracksAccessByVolume,"chapter" as access_level, j.chapter_id from `user_access_chapter_token` as `j` inner join `user_access_info` as `info` on `j`.`user_access_id` = `info`.`user_access_id` where ((j.from_ip <= 309824417 and j.to_ip >=309824417 )) and ((j.from_date <= 1740347465 and j.to_date >= 1740347465 and j.perpetual= 0) or (j.from_date is null and j.to_date is null and j.perpetual= 1)) and j.chapter_id = 6545)
      910μsalphaeurekaselec_live_10_06_2022UserAccess.php#1266
      Backtrace
      • 13. app/Models/UserAccess/UserAccess.php:1266
      • 14. app/Http/Controllers/ChapterController.php:1549
      • 15. vendor/laravel/framework/src/Illuminate/Routing/Controller.php:54
      • 16. vendor/laravel/framework/src/Illuminate/Routing/ControllerDispatcher.php:43
      • 17. vendor/laravel/framework/src/Illuminate/Routing/Route.php:260
    • select b.banner_link, b.banner_name, b.banner_script, b.banner_remarks, b.banner_file_name, b.banner_placement, bd.content_type, bd.content_id from `tbl_banner` as `b` inner join `tbl_banner_detail` as `bd` on `bd`.`banner_id` = `b`.`banner_id` inner join `users` as `u` on `u`.`id` = `b`.`updated_by` where `b`.`banner_ebook` = 1 and `bd`.`content_type` = 'B' and `bd`.`content_id` = 1519 and `b`.`banner_from_date` <= 1740347465 and `b`.`banner_to_date` >= 1740347465 and `b`.`banner_status` = 'A' order by `b`.`banner_id` desc
      1.46msalphaeurekaselec_live_10_06_2022Banner.php#95
      Bindings
      • 0: 1
      • 1: B
      • 2: 1519
      • 3: 1740347465
      • 4: 1740347465
      • 5: A
      Backtrace
      • 13. app/Models/Banner.php:95
      • 14. app/Http/helpers.php:404
      • 17. vendor/laravel/framework/src/Illuminate/Filesystem/Filesystem.php:124
      • 18. vendor/laravel/framework/src/Illuminate/View/Engines/PhpEngine.php:58
      • 19. vendor/laravel/framework/src/Illuminate/View/Engines/CompilerEngine.php:73
    • select count(*) as aggregate from `uc_cart_products` where cart_id='4421ae8e1f73bafeb73348095efe7d9d'
      270μsalphaeurekaselec_live_10_06_2022Cart.php#271
      Backtrace
      • 15. app/Models/Cart.php:271
      • 16. view::layouts._header:260
      • 18. vendor/laravel/framework/src/Illuminate/Filesystem/Filesystem.php:124
      • 19. vendor/laravel/framework/src/Illuminate/View/Engines/PhpEngine.php:58
      • 20. vendor/laravel/framework/src/Illuminate/View/Engines/CompilerEngine.php:73
    App\Models\Keywords
    5Keywords.php#?
    App\Models\Chapter
    1Chapter.php#?
    App\Models\Ebook
    1Ebook.php#?
        _token
        hpmCqn6hkklhsKi5WRt2oeZ30TzhLoGKANBflxBL
        uc_cart_id
        4421ae8e1f73bafeb73348095efe7d9d
        _previous
        array:1 [ "url" => "https://alpha.eurekaselect.com/chapter/6545" ]
        _flash
        array:2 [ "old" => [] "new" => [] ]
        PHPDEBUGBAR_STACK_DATA
        []
        path_info
        /chapter/6545
        status_code
        200
        
        status_text
        OK
        format
        html
        content_type
        text/html; charset=UTF-8
        request_query
        []
        
        request_request
        []
        
        request_headers
        0 of 0
        array:17 [ "x-https" => array:1 [ 0 => "1" ] "host" => array:1 [ 0 => "alpha.eurekaselect.com" ] "priority" => array:1 [ 0 => "u=0, i" ] "cookie" => array:1 [ 0 => "wayfindertarget=eyJpdiI6InVocWpRbWFIOWVyODQvOEFxSGNMZGc9PSIsInZhbHVlIjoibmNLaTlsd01Dd3VWcTMrRUEvdklZVVZKVStTYVNsSCtmZUhmMnpXNGRXOD0iLCJtYWMiOiI1MTFkZDVkYzQ1MWJjZmRkOGQ4M2M0YmM2NmFlYmU3MTEwYmRiNmQ5MTQ0YjJkYWViNzkyZTEyZGIxMzE1ZjEyIiwidGFnIjoiIn0%3Dwayfindertarget=eyJpdiI6InVocWpRbWFIOWVyODQvOEFxSGNMZGc9PSIsInZhbHVlIjoibmNLaTlsd01Dd3VWcTMrRUEvdklZVVZKVStTYVNsSCtmZUhmMnpXNGRXOD0iLCJtYWMiOiI1MTFkZDVkYzQ1MWJj" ] "accept-encoding" => array:1 [ 0 => "gzip, deflate, br, zstd" ] "sec-fetch-dest" => array:1 [ 0 => "document" ] "sec-fetch-user" => array:1 [ 0 => "?1" ] "sec-fetch-mode" => array:1 [ 0 => "navigate" ] "sec-fetch-site" => array:1 [ 0 => "none" ] "accept" => array:1 [ 0 => "text/html,application/xhtml+xml,application/xml;q=0.9,image/avif,image/webp,image/apng,*/*;q=0.8,application/signed-exchange;v=b3;q=0.7" ] "user-agent" => array:1 [ 0 => "Mozilla/5.0 AppleWebKit/537.36 (KHTML, like Gecko; compatible; ClaudeBot/1.0; +claudebot@anthropic.com)" ] "upgrade-insecure-requests" => array:1 [ 0 => "1" ] "sec-ch-ua-platform" => array:1 [ 0 => ""Windows"" ] "sec-ch-ua-mobile" => array:1 [ 0 => "?0" ] "sec-ch-ua" => array:1 [ 0 => ""HeadlessChrome";v="129", "Not=A?Brand";v="8", "Chromium";v="129"" ] "cache-control" => array:1 [ 0 => "no-cache" ] "pragma" => array:1 [ 0 => "no-cache" ] ]
        request_cookies
        0 of 0
        array:1 [ "wayfindertarget" => null ]
        response_headers
        0 of 0
        array:5 [ "content-type" => array:1 [ 0 => "text/html; charset=UTF-8" ] "cache-control" => array:1 [ 0 => "no-cache, private" ] "date" => array:1 [ 0 => "Sun, 23 Feb 2025 21:51:05 GMT" ] "set-cookie" => array:2 [ 0 => "XSRF-TOKEN=eyJpdiI6Ilh1cVltZHBzNzBLSnJCL0hHeUJsZEE9PSIsInZhbHVlIjoidzBsOFl2NDZKRHFjTTcvN3pRV3pab0ljdVVLM1h2bmlMbjFoVDRWalRBV1N6R0lVUDBSbVhDNkcyb1pxVVdzem9tSWM3QWFFK1BQOVhaMXVmSkZWY3ZyUm9BL0hHLzNEOE1udm8yQ00rc2cwSDZpYmhHeTJOMjdaRnhlMWhsMU0iLCJtYWMiOiJmNDBhMDUzMTU1MzA3YTk1YTRiYjBmNWNkYjQ3MjBmZDg5NmIyYjUxYTlhYjE1ZGFjMTE3Yjg5M2YzYTk1ZGJlIiwidGFnIjoiIn0%3D; expires=Wed, 26 Feb 2025 09:51:05 GMT; Max-Age=216000; path=/; secure; samesite=laxXSRF-TOKEN=eyJpdiI6Ilh1cVltZHBzNzBLSnJCL0hHeUJsZEE9PSIsInZhbHVlIjoidzBsOFl2NDZKRHFjTTcvN3pRV3pab0ljdVVLM1h2bmlMbjFoVDRWalRBV1N6R0lVUDBSbVhDNkcyb1pxVVdzem9tSWM3Q" 1 => "alphaeurekaselectnet_session=eyJpdiI6IlVMcDkwMkR1VWdqWC9ZelVkQU40cFE9PSIsInZhbHVlIjoiMkRIcTRuTTFFSnBPN1R6SmFmNFpSS2RHOGVTRnM0aDQzZjU2MjNnTUVvYVVLTmhYOW5jZnUzRTQ2aXVUVXJJMjVUays1VkthS3BjVnVKM2haVGJBNVdYbHowZlhkZnptWWpUbmNxM3FQS3Q0RG4wb1hlbDJOK2V2VERVcFIydGciLCJtYWMiOiJmZWIwOTU1OGI0YzhjMDBlNTI1NTA1MzI0MDdiYWE3MGRiODZjZTE4NWQ1ZWQ0Y2JjNDllOTgzZGYxYTUzNWU4IiwidGFnIjoiIn0%3D; path=/; secure; httponly; samesite=laxalphaeurekaselectnet_session=eyJpdiI6IlVMcDkwMkR1VWdqWC9ZelVkQU40cFE9PSIsInZhbHVlIjoiMkRIcTRuTTFFSnBPN1R6SmFmNFpSS2RHOGVTRnM0aDQzZjU2MjNnTUVvYVVLTmhYOW5jZnUzRTQ" ] "Set-Cookie" => array:2 [ 0 => "XSRF-TOKEN=eyJpdiI6Ilh1cVltZHBzNzBLSnJCL0hHeUJsZEE9PSIsInZhbHVlIjoidzBsOFl2NDZKRHFjTTcvN3pRV3pab0ljdVVLM1h2bmlMbjFoVDRWalRBV1N6R0lVUDBSbVhDNkcyb1pxVVdzem9tSWM3QWFFK1BQOVhaMXVmSkZWY3ZyUm9BL0hHLzNEOE1udm8yQ00rc2cwSDZpYmhHeTJOMjdaRnhlMWhsMU0iLCJtYWMiOiJmNDBhMDUzMTU1MzA3YTk1YTRiYjBmNWNkYjQ3MjBmZDg5NmIyYjUxYTlhYjE1ZGFjMTE3Yjg5M2YzYTk1ZGJlIiwidGFnIjoiIn0%3D; expires=Wed, 26-Feb-2025 09:51:05 GMT; path=/; secureXSRF-TOKEN=eyJpdiI6Ilh1cVltZHBzNzBLSnJCL0hHeUJsZEE9PSIsInZhbHVlIjoidzBsOFl2NDZKRHFjTTcvN3pRV3pab0ljdVVLM1h2bmlMbjFoVDRWalRBV1N6R0lVUDBSbVhDNkcyb1pxVVdzem9tSWM3Q" 1 => "alphaeurekaselectnet_session=eyJpdiI6IlVMcDkwMkR1VWdqWC9ZelVkQU40cFE9PSIsInZhbHVlIjoiMkRIcTRuTTFFSnBPN1R6SmFmNFpSS2RHOGVTRnM0aDQzZjU2MjNnTUVvYVVLTmhYOW5jZnUzRTQ2aXVUVXJJMjVUays1VkthS3BjVnVKM2haVGJBNVdYbHowZlhkZnptWWpUbmNxM3FQS3Q0RG4wb1hlbDJOK2V2VERVcFIydGciLCJtYWMiOiJmZWIwOTU1OGI0YzhjMDBlNTI1NTA1MzI0MDdiYWE3MGRiODZjZTE4NWQ1ZWQ0Y2JjNDllOTgzZGYxYTUzNWU4IiwidGFnIjoiIn0%3D; path=/; secure; httponlyalphaeurekaselectnet_session=eyJpdiI6IlVMcDkwMkR1VWdqWC9ZelVkQU40cFE9PSIsInZhbHVlIjoiMkRIcTRuTTFFSnBPN1R6SmFmNFpSS2RHOGVTRnM0aDQzZjU2MjNnTUVvYVVLTmhYOW5jZnUzRTQ" ] ]
        session_attributes
        0 of 0
        array:5 [ "_token" => "hpmCqn6hkklhsKi5WRt2oeZ30TzhLoGKANBflxBL" "uc_cart_id" => "4421ae8e1f73bafeb73348095efe7d9d" "_previous" => array:1 [ "url" => "https://alpha.eurekaselect.com/chapter/6545" ] "_flash" => array:2 [ "old" => [] "new" => [] ] "PHPDEBUGBAR_STACK_DATA" => [] ]
        ClearShow all
        Date ↕MethodURLData
        #12025-02-23 21:51:05GET/chapter/6545112197